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Strategies to Prevent Surgical Site Infections in Acute Care Hospitals: 2014 Update Author(s): Deverick J. Anderson, MD, MPH; Kelly Podgorny, DNP, MS, RN; Sandra I. Berríos- Torres, MD; Dale W. Bratzler, DO, MPH; E. Patchen Dellinger, MD; Linda Greene, RN, MPS, CIC; Ann-Christine Nyquist, MD, MSPH; Lisa Saiman, MD, MPH; Deborah S. Yokoe, MD, MPH; Lisa L. Maragakis, MD, MPH; Keith S. Kaye, MD, MPH Source: Infection Control and Hospital Epidemiology, Vol. 35, No. 6 (June 2014), pp. 605-627 Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiology of America Stable URL: http://www.jstor.org/stable/10.1086/676022 . Accessed: 12/12/2014 02:04 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . The University of Chicago Press and The Society for Healthcare Epidemiology of America are collaborating with JSTOR to digitize, preserve and extend access to Infection Control and Hospital Epidemiology. http://www.jstor.org This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AM All use subject to JSTOR Terms and Conditions

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Strategies to Prevent Surgical Site Infections in Acute Care Hospitals: 2014 UpdateAuthor(s): Deverick J. Anderson, MD, MPH; Kelly Podgorny, DNP, MS, RN; Sandra I. Berríos-Torres, MD; Dale W. Bratzler, DO, MPH; E. Patchen Dellinger, MD; Linda Greene, RN, MPS,CIC; Ann-Christine Nyquist, MD, MSPH; Lisa Saiman, MD, MPH; Deborah S. Yokoe, MD, MPH;Lisa L. Maragakis, MD, MPH; Keith S. Kaye, MD, MPHSource: Infection Control and Hospital Epidemiology, Vol. 35, No. 6 (June 2014), pp. 605-627Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiologyof AmericaStable URL: http://www.jstor.org/stable/10.1086/676022 .

Accessed: 12/12/2014 02:04

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

The University of Chicago Press and The Society for Healthcare Epidemiology of America are collaboratingwith JSTOR to digitize, preserve and extend access to Infection Control and Hospital Epidemiology.

http://www.jstor.org

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 2: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

infection control and hospital epidemiology june 2014, vol. 35, no. 6

s h e a / i d s a p r a c t i c e r e c o m m e n d a t i o n

Strategies to Prevent Surgical Site Infectionsin Acute Care Hospitals: 2014 Update

Deverick J. Anderson, MD, MPH;1 Kelly Podgorny, DNP, MS, RN;2 Sandra I. Berrıos-Torres, MD;3

Dale W. Bratzler, DO, MPH;4 E. Patchen Dellinger, MD;5 Linda Greene, RN, MPS, CIC;6

Ann-Christine Nyquist, MD, MSPH;7 Lisa Saiman, MD, MPH;8 Deborah S. Yokoe, MD, MPH;9

Lisa L. Maragakis, MD, MPH;10 Keith S. Kaye, MD, MPH11

Affiliations: 1. Duke University Medical Center, Durham, North Carolina; 2. The Joint Commission, Oakbrook Terrace, Illinois; 3. Centers for DiseaseControl and Prevention, Atlanta, Georgia; 4. University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; 5. University of WashingtonMedical Center, Seattle, Washington; 6. Highland Hospital and University of Rochester Medical Center, Rochester, New York; 7. Children’s Hospital Coloradoand University of Colorado School of Medicine, Aurora, Colorado; 8. Columbia University Medical Center, New York, New York; 9. Brigham and Women’sHospital and Harvard Medical School, Boston, Massachusetts; 10. Johns Hopkins University School of Medicine, Baltimore, Maryland; 11. Detroit MedicalCenter and Wayne State University, Detroit, Michigan.

Received February 12, 2014; accepted February 17, 2014; electronically published May 5, 2014.Infect Control Hosp Epidemiol 2014;35(6):605-627� 2014 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2014/3506-0001$15.00. DOI: 10.1086/676022

purpose

Previously published guidelines are available that provide com-prehensive recommendations for detecting and preventinghealthcare-associated infections (HAIs). The intent of this doc-ument is to highlight practical recommendations in a conciseformat designed to assist acute care hospitals in implementingand prioritizing their surgical site infection (SSI) preventionefforts. This document updates “Strategies to Prevent SurgicalSite Infections in Acute Care Hospitals,”1 published in 2008.This expert guidance document is sponsored by the Societyfor Healthcare Epidemiology of America (SHEA) and is theproduct of a collaborative effort led by SHEA, the InfectiousDiseases Society of America (IDSA), the American HospitalAssociation (AHA), the Association for Professionals in Infec-tion Control and Epidemiology (APIC), and The Joint Com-mission, with major contributions from representatives of anumber of organizations and societies with content expertise.The list of endorsing and supporting organizations is presentedin the introduction to the 2014 updates.2

section 1: rationale and statementsof concern

I. SSIs are common complications in acute care facilitiesA. SSIs occur in 2%–5% of patients undergoing inpatient

surgery.3,4

B. Approximately 160,000–300,000 SSIs occur each yearin the United States.5,6

C. SSI is now the most common and most costly HAI.7-9

II. Outcomes associated with SSIA. Up to 60% of SSIs have been estimated to be pre-

ventable by using evidence-based guidelines.10,11

B. SSIs account for 20% of all HAIs in hospitalizedpatients.12

C. Each SSI is associated with approximately 7–11 addi-tional postoperative hospital-days.3,9,13,14

D. Patients with an SSI have a 2–11-times higher risk ofdeath compared with operative patients without anSSI.15,16

1. Seventy-seven percent of deaths in patients with SSIare directly attributable to SSI.17

E. Attributable costs of SSI vary depending on the type ofoperative procedure and the type of infecting patho-gen.14,16,18-25

1. SSIs are believed to account for $3.5 billion to $10billion annually in healthcare expenditures using theCPI (consumer price index for inpatient hospital ser-vices with all cost estimates adjusted for 2007dollars).6

section 2: background—strategiesto detect ssi

I. Surveillance definitionsA. The Centers for Disease Control and Prevention’s

(CDC’s) National Healthcare Safety Network (NHSN)definitions for SSI are widely used for public reporting,interfacility comparison, and pay-for-performancecomparisons.26

B. SSIs are classified (Figure 1) as follows:1. Superficial incisional (involving only skin or subcu-

taneous tissue of the incision).

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figure 1. Centers for Disease Control and Prevention’s National Healthcare Safety Network classification for surgical site infection (SSI).215

2. Deep incisional (involving fascia and/or muscularlayers).a. Deep incision primary (DIP)—SSI identified in a

primary incision in a patient who has had an op-eration with 1 or more incisions.

b. Deep incision secondary (DIS)—SSI identified ina secondary incision in a patient who has had anoperation with more than 1 incision.

3. Organ/space (involving any part of the body openedor manipulated during the procedure, excluding skinincision, fascia, or muscle layers).

II. Methods for surveillance of SSIA. The direct method with daily observation of the surgical

site by the physician, physician extender, registerednurse, or infection prevention and control (IPC) pro-fessional starting 24–48 hours postoperatively is themost accurate method of surveillance.13,27-29

1. While the direct method is used as the gold standardfor studies, it is rarely used in practice because ofits resource utilization requirements and im-practicality.

B. The indirect method of SSI surveillance consists of acombination of the following:

1. Review of microbiology reports and patient medicalrecords.

2. Surgeon and/or patient surveys.3. Screening for readmission and/or return to the op-

erating room.4. Other information, such as coded diagnoses, coded

procedures, operative reports, or antimicrobialsordered.

C. The indirect method of SSI surveillance is less time-consuming and can be readily performed by IPC per-

sonnel during surveillance rounds.D. The indirect method of SSI surveillance is both reliable

(sensitivity, 84%–89%) and specific (specificity, 99.8%)compared with the gold standard of direct surveil-lance.30,31 Components of the indirect methods thatwere associated with highest sensitivities included re-view of nursing notes, International Classification of Dis-eases, Ninth Revision codes, and antimicrobials used.

E. Indirect methods for SSI surveillance are not reliablefor surveillance of superficial incisional infections, par-ticularly those occurring postdischarge.32

F. Automated data systems can be used to broaden SSIsurveillance.1. SSI surveillance can be expanded by utilizing hospital

databases that include administrative claims data (in-cluding diagnosis and procedure codes), antimicro-bial-days, readmission to the hospital, and return tothe operating room and/or by implementing a systemthat imports automated microbiologic culture data,surgical procedure data, and general demographic in-formation into a single surveillance database.33-35

2. These methods improve the sensitivity of indirect sur-veillance for detection of SSI and reduce the effortof the infection preventionist.33

3. Medicare claims data can be used to enhance tradi-tional surveillance methods for SSI and to identifyhospitals with unusually high or low rates of SSI.36,37

4. Use of administrative data can increase the efficiencyof SSI reporting and validation.38

III. Postdischarge surveillanceA. Over the past 3 decades, advances in medical technology

and changes in payment arrangements have increas-ingly shifted performance of surgical procedures from

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the acute care setting to the ambulatory (free-standingor hospital-affiliated) outpatient care setting.39-41

B. Concurrently, postoperative hospital length of stay hassteadily declined.42 These trends highlight the increasingimportance of postdischarge surveillance, withoutwhich SSI rates will be underestimated43 and oppor-tunities for improvements in healthcare delivery, patientsafety, and SSI prevention will be missed.

C. The proportion of SSIs detected through postdischargesurveillance can vary by surveillance method, operativesetting, type of SSI, and surgical procedure.

1. No standardized or reliable method for postdischargesurveillance has been established.34,44-48 Postdischargesurveillance based on surgeon and patient question-naire results have been shown to have poor sensitivityand specificity.44,49-51

2. The ambulatory care setting represents a challengebecause patients do not return to it for routine post-operative care or for management of complications.41

Research is needed to better understand how defi-nitions and postdischarge surveillance protocols de-veloped for the acute care setting can be translatedto the ambulatory care setting.

3. Superficial incisional SSIs are most commonly detectedand managed in the outpatient setting. In contrast,deep incisional and organ/space infections typically re-quire readmission to the hospital for management.32

4. In the Netherlands, the proportion of deep SSIs iden-tified after discharge from the hospital ranged from6% for colon resections to 88% for knee arthroplas-ties.43 The differences between these procedures couldbe explained by potential differences in both woundcontamination class and the duration of postdis-charge surveillance (30 days versus 1 year for animplant-related procedure). A pilot study in generalsurgery reported that 10.5% of SSIs following colonprocedures were identified after discharge from thehospital.52

5. By improving completeness of reporting, the overallinstitutional SSI rate typically increases after post-discharge surveillance methods are implemented re-gardless of which method is used.43,44,53

a. To improve interfacility comparisons and minimizepotential bias introduced by differences in post-discharge surveillance methods, national public re-porting focuses on nonsuperficial incisional SSIsdetected during hospitalization for the index pro-cedure or after discharge and requiring readmissionfor management.41,54,55

section 3: background—strategiesto prevent ssi

I. Summary of existing guidelines, recommendations, andrequirementsA. CDC and Healthcare Infection Control Practices Ad-

visory Committee (HICPAC) guidelines1. The most recently published guideline for prevention

of SSIs was released in 1999 by Mangram et al.17 TheCDC and HICPAC are currently working on an up-dated version of the guideline with a projected pub-lication date in mid-2014.

B. National Institute for Health and Clinical Excellence(NICE)—United Kingdom

1. NICE published guidelines for the prevention andtreatment of SSI in 2008.56

C. Surgical Infection Prevention (SIP) Project1. The Centers for Medicare & Medicaid Services (CMS)

created the SIP project in 2002.a. After review of published guidelines, an expert panel

identified 3 performance measures for quality im-provement related to antimicrobial prophylaxis:57,58

i. Delivery of intravenous antimicrobial prophy-laxis within 1 hour before incision (2 hours areallowed for the administration of vancomycinand fluoroquinolones).

ii. Use of an antimicrobial prophylactic agent con-sistent with published guidelines.

iii. Discontinuation of the prophylactic antimicro-bial agent within 24 hours after surgery (dis-continuation within 48 hours is allowable forcardiothoracic procedures in adult patients).

b. The SIP project focused on 7 procedures: abdom-inal hysterectomy, vaginal hysterectomy, hip ar-throplasty, knee arthroplasty, cardiac surgery, vas-cular surgery, and colorectal surgery.

c. Many hospitals that implemented and improvedcompliance with SIP performance measures de-creased their rates of SSI.59

D. Surgical Care Improvement Project (SCIP)1. The SCIP, a multiagency collaboration created in

2003, is an extension of SIP.2. In addition to the 3 performance measures of SIP,

the SCIP also focuses on 3 additional evidence-sup-ported process measures to prevent SSIs and ex-panded the types of operations eligible for the per-formance measures.58

a. Proper hair removal: no hair removal, althoughhair removal with clippers or the depilatorymethod is considered appropriate. Use of razors isconsidered inappropriate with exception of use onthe scrotal area or on the scalp after a traumatichead injury. Because of near-universal compliancewith this performance measure, CMS retired themeasure in 2012.

b. Controlling blood glucose during the immediatepostoperative period for cardiac surgery patients:controlled 6 am blood glucose (200 mg/dL orlower) on postoperative days 1 and 2, with theprocedure day being postoperative day 0. In 2014,this measure will be revised to assess glucose con-trol (180 mg/dL or lower) in cardiac surgery pa-

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tients in the time frame of 18–24 hours after an-esthesia end time.60,61

c. Maintenance of perioperative normothermia insurgical patients who have anesthesia duration ofat least 60 minutes.

E. Institute for Healthcare Improvement (IHI)1. The IHI created a nationwide quality improvement

project to improve outcomes in hospitalizedpatients.62,63

2. The IHI recommends the same 6 preventive measuresrecommended by the SCIP and has included these inthe 100,000 and 5 Million Lives Campaigns.62,63

F. The Joint Commission National Patient Safety Goals1. The Joint Commission’s National Patient Safety Goal

07.05.01 includes several evidence-based practices forprevention of SSI.64

G. Federal requirements1. CMS

a. In accordance with the Deficit Reduction Act of2005, hospitals that are paid by Medicare underthe Acute Care Inpatient Prospective Payment Sys-tem receive their full Medicare annual paymentupdate only if they submit required quality mea-sure information to CMS.

b. CMS now requires hospitals to submit data on 7SCIP measures as a part of the Hospital InpatientQuality Reporting (IQR) system.65 Three of thesemeasures focus on prevention of SSI (antimicrobialprophylaxis provided within 1 hour of incision,antimicrobial selection, and cardiac surgery peri-operative glucose control). In addition, CMS nowrequires hospitals to report SSI rates for patientsundergoing abdominal hysterectomy and colorec-tal surgery through NHSN.65

c. Actual rates of performance on SCIP measures nowimpacts hospital payment under the Value-BasedPurchasing (VBP) program. Current benchmarksidentified for the VBP score that is used to modifya hospital’s base operating diagnosis-related grouppayment are at or near 100%.65,66

II. Infrastructure requirementsA. Trained personnel

1. Infection preventionists must (1) be specificallytrained in methods of SSI surveillance, (2) haveknowledge of and the ability to prospectively applythe CDC/NHSN definitions for SSI, (3) possess basiccomputer and mathematical skills, and (4) be adeptat providing feedback and education to healthcarepersonnel when appropriate.17

B. Education1. Regularly provide education to surgeons and periop-

erative personnel through continuing education ac-tivities directed at minimizing perioperative SSI riskthrough implementation of recommended processmeasures.

a. Several educational components can be combinedinto concise, efficient, and effective recommenda-tions that are easily understood and remembered.67

b. Provide education regarding the outcomes asso-ciated with SSI, risks for SSI, and methods to re-duce risk to all patients, patients’ families, sur-geons, and perioperative personnel.

c. Education for patients and patients’ families is aneffective method to reduce risk associated with in-trinsic patient-related SSI risk factors.68,69

C. Computer-assisted decision support and automatedreminders

1. Several institutions have successfully employed com-puter-assisted decision support methodology to im-prove the rate of appropriate administration of an-timicrobial prophylaxis (including redosing duringprolonged cases).70-73

2. Computer-assisted decision support, however, is po-tentially expensive, can be time-consuming to im-plement, and in a single study was reported to initiallyincrease the rate of adverse drug reactions.74

3. Institutions must appropriately validate computer-as-sisted decision support systems after implementation.

D. Utilization of automated data1. Install information technology infrastructure to fa-

cilitate data transfer, receipt, and organization to aidwith tracking of process and outcome measures.

section 4: recommended strategiesfor ssi prevention

Recommendations are categorized as either (1) basic practicesthat should be adopted by all acute care hospitals or (2)special approaches that can be considered for use in locationsand/or populations within hospitals when HAIs are not con-trolled by use of basic practices. Basic practices include rec-ommendations where the potential to impact HAI risk clearlyoutweighs the potential for undesirable effects. Special ap-proaches include recommendations where the intervention islikely to reduce HAI risk but where there is concern aboutthe risks for undesirable outcomes resulting from the inter-vention, where the quality of evidence is low, or where evi-dence supports the impact of the intervention in select set-tings (eg, during outbreaks) or for select patient populations.Hospitals can prioritize their efforts by initially focusing onimplementation of the prevention approaches listed as basicpractices. If HAI surveillance or other risk assessments suggestthat there are ongoing opportunities for improvement, hos-pitals should then consider adopting some or all of the pre-vention approaches listed as special approaches. These canbe implemented in specific locations or patient populationsor can be implemented hospital-wide, depending on outcomedata, risk assessment, and/or local requirements. Each infec-

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table 1. Grading of the Quality of Evidence

Grade Definition

I. High Highly confident that the true effect lies close to that of the estimated size and direction of theeffect. Evidence is rated as high quality when there is a wide range of studies with no majorlimitations, there is little variation between studies, and the summary estimate has a narrowconfidence interval.

II. Moderate The true effect is likely to be close to the estimated size and direction of the effect, but there isa possibility that it is substantially different. Evidence is rated as moderate quality when thereare only a few studies and some have limitations but not major flaws, there is some variationbetween studies, or the confidence interval of the summary estimate is wide.

III. Low The true effect may be substantially different from the estimated size and direction of the effect.Evidence is rated as low quality when supporting studies have major flaws, there is importantvariation between studies, the confidence interval of the summary estimate is very wide, orthere are no rigorous studies, only expert consensus.

note. Based on Grades of Recommendation, Assessment, Development, and Evaluation (GRADE)234 and theCanadian Task Force on Preventive Health Care.235

tion prevention recommendation is given a quality-of-evi-dence grade (see Table 1).

I. Basic practices for preventing SSI: recommended for allacute care hospitals1. Administer antimicrobial prophylaxis according to evi-

dence-based standards and guidelines (quality of evi-dence: I).17,75,76

a. Begin administration within 1 hour before incisionto maximize tissue concentration.57,58 Administeringagent closer than 1 hour is effective, and some studiesshow superior efficacy for administration between 0and 30 minutes prior to incision compared with ad-ministration between 30 and 60 minutes.77,78

i. Two hours are allowed for the administration ofvancomycin and fluoroquinolones.

ii. Many experts believe that antimicrobials should beinfused prior to inflation of tourniquets in proce-dures using “bloodless” techniques, although dataare insufficient to support this recommendation.79,80

b. Select appropriate agents on the basis of the surgicalprocedure, the most common pathogens causing SSIsfor a specific procedure, and published recommen-dations.76

c. Discontinue agent within 24 hours after surgery.76

i. Although guidelines suggest stopping the antimi-crobial agent within 24 hours of surgery, there isno evidence that agents given after closure con-tribute to efficacy, and they do contribute to in-creased resistance81,82 and the risk of Clostridiumdifficile disease.83

d. Adjust dosing on the basis of patient weight;76 forexample:i. Use 30 mg/kg for pediatric patients, 2 g of cefa-

zolin for patients weighing 80 kg or more, and 3g for patients weighing 120 kg or more.

ii. Vancomycin should be dosed at 15 mg/kg.iii. Gentamicin should be dosed at 5 mg/kg for adult

patients and 2.5 mg/kg for pediatric patients.(a) For morbidly obese patients receiving genta-

micin, the weight used for dose calculationshould be the ideal weight plus 40% of theexcess weight.

e. Redose prophylactic antimicrobial agents for longprocedures and in cases with excessive blood loss dur-ing the procedure.76

i. Prophylactic antimicrobials should be redosed atintervals of 2 half-lives (measured from time thepreoperative dose was administered) in cases thatexceed this time.

f. Use a combination of parenteral antimicrobial agentsand oral antimicrobials to reduce the risk of SSI fol-lowing colorectal procedures.84-91

i. The additional SSI reduction achieved with me-chanical bowel preparation has not been studied,but the data supporting use of oral antimicrobialshave all been generated in combination with me-chanical bowel preparation.

ii. Mechanical bowel preparation without oral anti-microbials does not decrease the risk of SSI.92

2. Do not remove hair at the operative site unless thepresence of hair will interfere with the operation. Donot use razors (quality of evidence: II).17,93

a. If hair removal is necessary, remove hair outside theoperating room using clippers or a depilatory agent.

3. Control blood glucose during the immediate postop-erative period for cardiac surgery patients58 (quality ofevidence: I) and noncardiac surgery patients94-98 (qualityof evidence: II).a. Maintain postoperative blood glucose of 180 mg/dL

or lower.i. The recommendation of maintaining postoperative

blood glucose less than 200 mg/dL at 6 am on post-operative days 1 and 2 is being replaced. In 2014,this measure will be revised in the SCIP to assess

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glucose control (180 mg/dL or lower) in cardiacsurgery patients in the time frame of 18–24 hoursafter anesthesia end time. Several societies, experts,and the National Quality Forum support this newrecommendation.60,61,99,100

b. Intensive postoperative glucose control (targeting lev-els less than 110 mg/dL) has not been shown to re-duce the risk of SSI and may actually lead to higherrates of adverse outcomes, including stroke anddeath.101

4. Maintain normothermia (temperature of 35.5�C ormore) during the perioperative period (quality of evi-dence: I).a. Even mild degrees of hypothermia can increase SSI

rates. Hypothermia may directly impair neutrophilfunction or impair it indirectly by triggering subcu-taneous vasoconstriction and subsequent tissue hyp-oxia. In addition, hypothermia may increase bloodloss, leading to wound hematomas or need for trans-fusion, both of which can increase rates of SSI.102

b. Randomized controlled trials have shown the benefitsof both preoperative and intraoperative warming toreduce SSI rates and to reduce intraoperative bloodloss.103-105

5. Optimize tissue oxygenation by administering supple-mental oxygen during and immediately following sur-gical procedures involving mechanical ventilation (qual-ity of evidence: I).a. Supplemental oxygen is most effective when com-

bined with additional strategies to improve tissue oxy-genation, including maintenance of normothermiaand appropriate volume replacement. The availableevidence is in patients undergoing surgery with gen-eral anesthesia using mechanical ventilation.106-108

i. Seven randomized clinical trials have been pub-lished comparing 80% with 30%–35% FiO2 (4with nitrogen106-109 and 3 with nitrous oxide110-112)in patients undergoing general anesthesia with in-traoperative mechanical ventilation and postop-erative oxygen delivered for 2–6 hours via a non-rebreathing mask.

ii. Three trials in patients undergoing elective colo-rectal resection106,107,111 and 1 each in open appen-dectomy108 and total gastrectomy with esophago-jejunal anastomosis112 reported an approximate40% decrease in the rate of SSI. Three of the studiesreported protocols that included maintenance ofperioperative normothermia and liberal fluid re-placement.106-108

iii. Two trials in mixed surgical populations under-going emergency or elective laparotomy for gas-trointestinal, gynecologic, or urologic proceduresreported different results.109,110

(a) The large multicenter trial that restricted peri-operative fluid replacement reported no dif-

ference.109 A follow-up study performed in thispopulation noted that patients undergoingcancer surgery who received 80% FiO2 hadhigher rates of mortality than patients under-going cancer surgery who received 30%FiO2.

113

(b) The smaller trial without standardized proto-cols for perioperative normothermia or volumereplacement reported an increase in SSIs.110 Inthis study, the 80% FiO2 group had a signifi-cantly higher proportion of patients with highbody mass index (more than 30), higher bloodloss, more crystalloid infused, and longer op-erations. This group also had 5 patients whoremained intubated postoperatively (vs 1 in the35% group). Postoperative intubation was pre-dictive of SSI.

b. A meta-analysis of 5 of the above-referenced studiesconcluded that perioperative supplemental oxygenled to a relative risk (RR) reduction of 25% for SSI.114

6. Use alcohol-containing preoperative skin preparatoryagents if no contraindication exists (quality of evi-dence: I).a. Alcohol is highly bactericidal and effective for pre-

operative skin antisepsis but does not have persistentactivity when used alone. Rapid, persistent, and cu-mulative antisepsis can be achieved by combining al-cohol with chlorhexidine gluconate or an iodophor.115

i. Alcohol is contraindicated for certain procedures,including procedures in which the preparatoryagent may pool or not dry (eg, involving hair) dueto fire risk. Alcohol may also be contraindicatedfor procedures involving mucosa, cornea, or ear.

b. The most effective disinfectant to combine with al-cohol is unclear.i. A recent trial of 849 patients undergoing clean-

contaminated surgery randomized patients to pre-operative skin antisepsis with chlorhexidine-alcohol or povidone-iodine.116 The overall rate ofSSI was significantly lower in the chlorhexidine-alcohol group than in the povidone-iodine group(9.5% vs 16% [P p .004]; RR, 0.59 [95% con-fidence interval (CI), 0.41–0.85]).

ii. In contrast, a single-center study compared pov-idone-iodine followed by isopropyl alcohol versuschlorhexidine-alcohol versus iodine-alcohol usinga sequential implementation design.117 Generalsurgical patients who received skin antisepsis withiodine-alcohol had the lowest rates of SSI (3.9 per100 procedures), compared with 6.4 per 100 pro-cedures for patients who received povidone-iodinefollowed by alcohol and 7.1 per 100 proceduresfor patients who received chlorhexidine-alcohol.

iii. In the absence of alcohol, chlorhexidine gluconatemay have advantages over povidone-iodine, in-

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cluding longer residual activity and activity in thepresence of blood or serum.118,119

iv. These disinfectants are not interchangeable. Fol-low the manufacturers’ instructions to ensure cor-rect application.

7. Use impervious plastic wound protectors for gastroin-testinal and biliary tract surgery (quality of evidence: I).a. A wound protector is a plastic sheath that lines a

wound and can facilitate retraction of an incisionduring surgery without the need for additional me-chanical retractors.

b. A recent meta-analysis of 6 randomized clinical trialsin 1,008 patients reported that use of a plastic woundprotectors was associated with a 45% decrease inSSIs.120

i. There was a nonsignificant trend toward greaterprotective effect using a dual-ring protector com-pared with a single-ring protector.

8. Use a checklist based on the World Health Organization(WHO) checklist to ensure compliance with best prac-tices to improve surgical patient safety (quality of evi-dence: I).a. The WHO checklist is a 19-item surgical safety check-

list to improve adherence with best practices.b. A multicenter quasi-experimental study conducted in

8 countries demonstrated that use of the WHOchecklist led to lower rates of surgical complications,including SSI and death.121

c. These findings have been confirmed in subsequentsingle-center and multicenter quasi-experimentalstudies.122,123

9. Perform surveillance for SSI (quality of evidence: II).a. Identify high-risk, high-volume operative procedures

to be targeted for SSI surveillance on the basis of arisk assessment of patient populations, operative pro-cedures performed, and available SSI surveillancedata.

b. Identify, collect, store, and analyze data needed forthe surveillance program.17

i. Develop a database for storing, managing, andaccessing data collected on SSIs.

ii. Implement a system for collecting data needed toidentify SSIs. Data are required from surgical andmicrobiological databases. Obtain the followingdata from surgical databases: patient name, med-ical record number, date, type of procedure, sur-geons, anesthesiologists, incision time, woundclass, ASA score, closure time, and presence of anSSI. Ideally, these data are supplemented with pro-cess data, including prophylactic agent and doseand time(s) of administration of prophylacticagent. For patients diagnosed with an SSI, nec-essary microbiological data include type of SSI,infecting organism and antimicrobial susceptibil-ities, and date of infection. More detailed surgical

and patient information may be useful for someprocedures, including use of general anesthesia,emergency or trauma-related surgery, body massindex, and diagnosis of diabetes.

iii. Prepare periodic SSI reports (time frame will de-pend on hospital needs and volume of targetedprocedures).

iv. Collect denominator data on all patients under-going targeted procedures in order to calculate SSIrates for each type of procedure.67

v. Identify trends (eg, in SSI rates and pathogenscausing SSIs).

c. Use updated CDC NHSN definitions for SSI.26

d. Perform indirect surveillance for targeted pro-cedures.30,31,124,125

e. Perform postoperative surveillance for 30 days; ex-tend the postoperative surveillance period to 90 daysfor certain procedure categories.26

i. Procedures that require 90-day surveillance are de-termined by specific procedure codes.

f. Surveillance should be performed on patients re-admitted to the hospital.i. If an SSI is diagnosed at your institution but the

surgical procedure was performed elsewhere, notifythe hospital where the original procedure wasperformed.

g. Develop a system for routine review and interpre-tation of SSI rates to detect significant increases oroutbreaks and to identify areas where additional re-sources might be needed to improve SSI rates.125 Ifincreased rates are identified, determine the numberof potentially preventable infections that occurred,defined as the number of SSIs that occurred duringa procedure in which less than 100% of recommendedpractices and processes were completed.

10. Increase the efficiency of surveillance through utili-zation of automated data (quality of evidence: II).

a. Implement a method to electronically transfer mi-crobiology and operative data, including process mea-sures when available, to IPC personnel to facilitatedenominator data acquisition and calculation of SSIrates for various procedures.

b. If information technology and infrastructure re-sources are available, develop automated methodsfor detection of SSIs utilizing automated data forreadmissions, diagnosis and procedure codes, mi-crobiology results, and antimicrobial dispens-ing.35,126-129

c. Implementation of automated surveillance may im-prove the sensitivity of surveillance.

11. Provide ongoing feedback of SSI rates to surgical andperioperative personnel and leadership (quality of evi-dence: II).

a. Routinely audit and provide confidential feedback onSSI rates and adherence to process measures to in-

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dividual surgeons, the surgical division and/or de-partment chiefs, and hospital leadership.17,130

i. For each type of procedure performed, providerisk-adjusted rates of SSI.

ii. Anonymously benchmark procedure-specific risk-adjusted rates of SSI among peer surgeons.

12. Measure and provide feedback to providers regardingrates of compliance with process measures (quality ofevidence: III).58

a. Routinely provide feedback to surgical staff, periop-erative personnel, and leadership regarding compli-ance with targeted process measures.

13. Educate surgeons and perioperative personnel aboutSSI prevention (quality of evidence: III).

a. Include risk factors, outcomes associated with SSI,local epidemiology (eg, SSI rates by procedure, rateof methicillin-resistant Staphylococcus aureus [MRSA]infection in a facility), and basic prevention measures.

14. Educate patients and their families about SSI preven-tion as appropriate (quality of evidence: III).

a. Provide instructions and information to patientsprior to surgery describing strategies for reducing SSIrisk. Specifically provide preprinted materials topatients.131

b. Examples of printed materials for patients are avail-able from the following websites:i. JAMA patient page: wound infections (from the

Journal of the American Medical Association; avail-able at http://jama.ama-assn.org/cgi/reprint/294/16/2122).

ii. SCIP’s tips for safer surgery (available at https://www.premierinc.com/safety/topics/scip/downloads/consumer-tips.pdf).

iii. Frequently asked questions about SSIs (availablefrom SHEA at http://www.shea-online.org/Assets/files/patient%20guides/NNL_SSI.pdf).

iv. SSI: resources for patients and healthcare provid-ers (available from the CDC at http://www.cdc.gov/hai/ssi/ssi.html).

15. Implement policies and practices aimed at reducingthe risk of SSI that align with evidence-based standards(eg, CDC, Association for periOperative RegisteredNurses, and professional organization guidelines; qual-ity of evidence: II).17,58,132

a. The pathogenesis and likelihood of developing an SSIinvolves a complex relationship among the following:i. Microbial characteristics (eg, degree of contami-

nation, virulence of pathogen);ii. Patient characteristics (eg, immune status, co-

morbid conditions); andiii. Surgical characteristics (eg, type of procedure, in-

troduction of foreign material, amount of damageto tissues).133

b. Risk factors for SSI can be separated into intrinsicpatient-related characteristics and extrinsic proce-

dure-related characteristics. Implement policies andpractices to reducing modifiable risk factors (Table2), including the following:i. Optimal preparation and disinfection of the op-

erative site and the hands of the surgical teammembers.

ii. Adherence to hand hygiene, including nonsurgeonmembers of the operating team.134

iii. Reduce unnecessary traffic in operatingrooms.135,136

iv. Appropriate care and maintenance of operatingrooms, including appropriate air handling and op-timal cleaning and disinfection of equipment andthe environment.17

II. Special approaches for preventing SSIStandard infection control methods of outbreak inves-

tigation are recommended for use in locations and/orpopulations within the hospital with unacceptably highSSI rates despite implementation of the basic SSI preven-tion strategies listed above.

1. Screen for S. aureus and decolonize surgical patientswith an antistaphylococcal agent in the preoperative set-ting for high-risk procedures, including some ortho-pedic and cardiothoracic procedures (quality of evi-dence: II).a. Screening for S. aureus refers to the practice of at-

tempting to identify patients colonized with methi-cillin-susceptible S. aureus (MSSA) and/or MRSA.Decolonization refers to the practice of treating pa-tients with known S. aureus colonization with anti-microbial and/or antiseptic agents to eliminate S. au-reus colonization.i. There is no standardized approach to either screen-

ing or decolonizing. Most clinicians attempt to de-colonize surgical patients with a combination ofchlorhexidine gluconate applied to the skin and na-sal mupirocin.

b. A Cochrane review concluded that mupirocin alonemay be effective, particularly in certain groups, in-cluding orthopedic and cardiothoracic patients.137

Several nonrandomized trials corroborate this con-clusion.138-140

c. Clinical practice guidelines from the American So-ciety of Health-System Pharmacists recommend giv-ing mupirocin intranasally to all patients with doc-umented S. aureus colonization for orthopedicprocedures, including total joint replacement and hipfracture repair, and cardiac procedures.76

d. Some trials demonstrate that preoperative screeningfor S. aureus, coupled with intranasal mupirocin andchlorhexidine bathing is effective in reducing SSI forsome patients.

i. For example, a randomized, double-blind, placebo-controlled, multicenter trial that evaluated rapididentification of S. aureus nasal carriers followed

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table 2. Selected Risk Factors for and Recommendations to Prevent Surgical Site Infections (SSIs)

Risk factor RecommendationQuality

of evidence

Intrinsic, patient related (preoperative)Unmodifiable

Age No formal recommendation. Relationship to increased risk of SSI may besecondary to comorbidities or immunosenescence.216-218

NA

History of radiation No formal recommendation. Prior irradiation at the surgical site increasesthe risk of SSI, likely due to tissue damage and wound ischemia.219

NA

History of SSTIs No formal recommendation. History of a prior skin infection may be amarker for inherent differences in host immune function.220

NA

ModifiableGlucose control Control serum blood glucose levels for all surgical patients, including pa-

tients without diabetes.17 For patients with diabetes mellitus, reduceglycosylated hemoglobin A1c levels to less than 7% before surgery,if possible.94

I

Obesity Increase dosing of prophylactic antimicrobial agent for morbidly obesepatients.76,221

I

Smoking cessation Encourage smoking cessation within 30 days of procedure.17,222-226 IImmunosuppressive medications Avoid immune-suppressive medications in perioperative period, if possible. IIIHypoalbuminemia No formal recommendation. Although a noted risk factor,227 do not delay

surgery for use of TPN.NA

Extrinsic, procedure related (perioperative)Preparation of patient

Hair removal Do not remove unless hair will interfere with the operation.17 If hair re-moval is necessary, remove outside the OR by clipping. Do not userazors.

II

Preoperative infections Identify and treat infections (eg, urinary tract infection) remote to the sur-gical site prior to elective surgery.17 Do not routinely treat colonizationor contamination.

II

Operative characteristicsSurgical scrub (surgical team members’

hands and forearms)Use appropriate antiseptic agent to perform preoperative surgical

scrub.17,228 For most products, scrub the hands and forearms for 2–5minutes.

II

Skin preparation Wash and clean skin around incision site. Use a dual agent skin prepara-tion containing alcohol, unless contraindications exist.17

I

Antimicrobial prophylaxis Administer only when indicated.17 ITiming Administer within 1 hour of incision to maximize tissue concentration76,a IBlood transfusion Blood transfusions increase the risk of SSI by decreasing macrophage

function. Reduce blood loss and need for blood transfusion to thegreatest extent possible.229-231

II

Choice of prophylactic agent Select appropriate agents on the basis of surgical procedure, most com-mon pathogens causing SSIs for a specific procedure, and publishedrecommendations.76

I

Duration of prophylaxis Stop agent within 24 hours after the procedure for all procedures.76 IISurgeon skill/technique Handle tissue carefully and eradicate dead space.17 IIIAppropriate gloving All members of the operative team should double glove and change gloves

when perforation is noted.208

III

Asepsis Adhere to standard principles of OR asepsis.17 IIIOperative time No formal recommendation in most recent guidelines. Minimize as much

as possible without sacrificing surgical technique and aseptic practice.I

OR characteristicsVentilation Follow American Institute of Architects’ recommendations for proper air

handling in the OR.17,232

III

Traffic Minimize OR traffic.17,135,136 IIIEnvironmental surfaces Use an EPA-approved hospital disinfectant to clean visibly soiled or con-

taminated surfaces and equipment.17

III

Sterilization of surgical equipment Sterilize all surgical equipment according to published guidelines.233 Mini-mize the use of immediate-use steam sterilization.17

II

note. EPA, Environmental Protection Agency; NA, not applicable; OR, operating room; SSTI, skin and soft-tissue infection; TPN, totalparenteral nutrition.a Vancomycin and fluoroquinolones can be given 2 hours prior to incision.

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by decolonization was associated with a greater than2-fold reduction in the risk for postoperative in-fection due to S. aureus and an almost 5-fold re-duction in risk for deep incisional SSI due to S.aureus.141

(a) This study was performed in a setting with highbaseline rates of SSI and in the absence ofMRSA.

e. In contrast, other trials have failed to demonstrate abenefit.i. A prospective, interventional cohort study with a

crossover design involving 21,000 patients con-cluded that universal, rapid screening for MRSAat admission coupled with decolonization of car-riers did not reduce the rate of SSI due to MRSA.142

ii. A double-blind randomized controlled trial in-volving more than 4,000 patients showed that in-tranasal application of mupirocin, which was notcoupled with chlorhexidine bathing, did not sig-nificantly reduce the S. aureus SSI rate.143

(a) In a secondary analysis of these data, the useof intranasal mupirocin was associated with anoverall decreased rate of nosocomial S. aureusinfections among the S. aureus carriers.

f. A recently published meta-analysis of 17 studies con-cluded that decolonization strategies prevent gram-positive SSIs, S. aureus SSIs, and MRSA SSIs, althoughthere was significant heterogeneity among the trials.144

g. Factors that impact the decision to implement screen-ing for S. aureus and decolonization include adher-ence to basic SSI prevention strategies, baseline rateof SSI due to S. aureus, individual patient risk factorsfor acquiring SSI due to S. aureus, availability of re-sources to implement the protocol, and ability to fol-low-up on protocol parameters (eg, laboratory re-sults) and adherence.

h. Routine preoperative decolonization with mupirocinwithout screening is not currently recommended.

i. Mupirocin resistance has been documented.145

2. Perform antiseptic wound lavage (quality of evidence: II).a. Wound lavage is a common practice, although the

solution used for lavage differs among surgeons.146

b. Several groups have evaluated whether dilute povi-done-iodine lavage of the surgical wound can de-crease the risk of SSI. A meta-analysis published in2010 evaluated 24 randomized controlled trials andconcluded that lavage with dilute povidone-iodinedecreased the risk of SSI compared with nonantisepticlavage (RR, 0.64 [95% CI, 0.51–0.82]).147

3. Perform an SSI risk assessment (quality of evidence: III).a. Convene a multidisciplinary team (eg, surgical lead-

ership, hospital administration, quality managementservices, and infection control) to identify gaps, im-prove performance, measure compliance, assess im-pact of interventions, and provide feedback.148

b. Determine baseline SSI rates by surgical specialty,procedure, and/or surgeon to better target your eval-uation and interventions.

4. Observe and review operating room personnel and theenvironment of care in the operating room (quality ofevidence: III).a. Perform direct observation audits of operating room

personnel to assess operating room processes andpractices to identify infection control lapses, includ-ing but not limited to adherence to process measures(antimicrobial prophylaxis choice, timing and dura-tion protocols, hair removal, etc), surgical hand an-tisepsis, patient skin preparation, operative technique,surgical attire (wearing and/or laundering outside theoperating room), and level of operating room traf-fic.149-153 Perform remediation when breaches of stan-dards are identified.i. Operating room personnel should include sur-

geons, surgical technologists, anesthesiologists, cir-culating nurses, residents, medical students, train-ees, and device manufacturer representatives.149

b. Perform direct-observation audits of environmentalcleaning practices in the operating room, instrumentprocessing (sterilization), and storage facilities.i. Review instrument processing and flash steriliza-

tion logs.ii. Review maintenance records for operating room

heating, ventilation, and air conditioning system,including results of temperature and relative hu-midity testing, and test for maintenance of positiveair pressure in the operating room(s).

c. Provide feedback and review infection control mea-sures with operating room and environmentalpersonnel.

5. Observe and review practices in the postanesthesia careunit, surgical intensive care unit, and/or surgical ward(quality of evidence: II).a. Perform direct observation audits of hand hygiene

practices among all personnel with direct patientcontact.151

b. Evaluate wound care practices.154

c. Perform direct observation audits of environmentalcleaning practices.

d. Provide feedback and review infection control mea-sures with staff in these postoperative care settings.

III. Approaches that should not be considered a routine partof SSI prevention

1. Do not routinely use vancomycin for antimicrobial pro-phylaxis (quality of evidence: II).75,76,155

a. Vancomycin should not routinely be used for anti-microbial prophylaxis, but it can be an appropriateagent for specific scenarios. Reserve vancomycin forspecific clinical circumstances, such as a proven out-break of SSI due to MRSA; high endemic rates of SSIdue to MRSA; targeted high-risk patients who are at

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increased risk for SSI due to MRSA (including car-diothoracic surgical patients and elderly patients withdiabetes); and high-risk surgical procedures in whichan implant is placed.156

i. No definitions for high endemic rates of SSI dueto MRSA have been established.157

ii. Studies of the efficacy of vancomycin prophylaxiswere published prior to the emergence of com-munity-acquired MRSA.

b. Two meta-analyses of studies comparing glycopeptidesto b-lactam antimicrobial prophylaxis concluded thatthere was no difference in rates of SSI between the 2antimicrobial prophylaxis regimens.144,158

c. A meta-analysis of 6 studies concluded that prophylaxiswith a glycopeptide and a second agent was protectiveagainst SSI due to gram-positive organisms comparedwith prophylaxis with a b-lactam alone.144 Of note, the2 randomized controlled trials included in the meta-analysis combined a glycopeptide with non-b-lactamantibiotic(s). Thus, no study has prospectively analyzedthe effect of providing both glycopeptides and b-lactamantimicrobials for preoperative antimicrobial prophy-laxis. As vancomycin does not have activity againstgram-negative pathogens and appears to have less ac-tivity against MSSA than b-lactam agents, many expertsrecommend adding vancomycin to standard antimi-crobial prophylaxis for the specific clinical circum-stances described above.76,157-159

2. Do not routinely delay surgery to provide parenteralnutrition (quality of evidence: I).a. Preoperative administration of total parenteral nu-

trition has not been shown to reduce the risk of SSIin prospective randomized controlled trials and mayincrease the risk of SSI.160,161

b. Individual trials comparing enteral and parenteralperioperative nutrition and “immunomodulating”diets containing arginine and/or glutamine with“standard” control diets tend to have very small num-bers and fail to show significant differences. Two re-cent meta-analyses, however, demonstrate reductionin postoperative infectious complication in patientsreceiving enteral diets containing glutamine and/orarginine administered either before or after the sur-gical procedure.162,163

3. Do not routinely use antiseptic-impregnated sutures asa strategy to prevent SSIs (quality of evidence: II).a. Human volunteer studies involving foreign bodies

have demonstrated that the presence of surgical su-tures decreases the inoculum required to cause an SSIfrom 106 to 102 organisms.164

b. Some trials have shown that surgical wound closurewith triclosan-coated polygactin 910 antimicrobialsutures may decrease the risk of SSI compared withstandard sutures. For example, a recent randomizedcontrolled trial of 410 colorectal surgeries concluded

that the rate of SSI decreased more than 50% (9.3%in the control group vs 4.3% among cases; P p .05).165

c. In contrast, a recent systematic review and meta-anal-ysis evaluated 7 randomized clinical trials and con-cluded that neither rates of SSI (odds ratio [OR], 0.77[95% CI, 0.4–1.51]; P p .45) nor rates of wounddehiscence (OR, 1.07 [95% CI, 0.21–5.43]; P p .93)were statistically different compared with controls.166

In addition, one small study raised concern abouthigher rates of wound dehiscence while using thesesutures.167

d. The impact of routine use of antiseptic-impregnatedsutures on development of resistance to antisepticsis unknown.

4. Do not routinely use antiseptic drapes as a strategy toprevent SSIs (quality of evidence: I).a. An incise drape is an adhesive film that covers the

surgical incision site to minimize bacterial woundcontamination due to endogenous flora. These drapescan be impregnated with antiseptic chemicals, suchas iodophors.

b. A 2007 Cochrane review of 5 trials concluded thatnonantiseptic incise drapes were associated with ahigher risk of SSI compared with no incise drape (RR,1.23 [95% CI, 1.02–1.48]),168 although this associa-tion may have been caused by one specific study.169

Two trials (abdominal and cardiac surgical patients)compared iodophor-impregnated drapes to nodrapes.170,171 While wound contamination was de-creased in one trial,170 neither trial demonstrated thatiodophor-impregnated drapes decreased the rate ofSSI. A nonrandomized retrospective study similarlyconcluded that impregnated drapes do not preventSSIs after hernia repair.172

IV. Unresolved issues1. Preoperative bathing with chlorhexidine-containing

products.a. Preoperative bathing with agents such as chlorhexi-

dine has been shown to reduce bacterial colonizationof the skin.173 Several studies have examined the utilityof preoperative showers, but none has definitivelyproven that they decrease SSI risk. A Cochrane reviewevaluated the evidence for preoperative bathing orshowering with antiseptics for SSI prevention.174 Sixrandomized controlled trials evaluating the use of 4%chlorhexidine gluconate were included in the analysis,with no clear evidence of benefit noted. It should benoted that several of these studies had methodologicallimitations and were conducted several years ago.Thus, the role of preoperative bathing in SSI preven-tion is still uncertain.i. To gain the maximum antiseptic effect of chlor-

hexidine, adequate levels of CHG must be achievedand maintained on the skin. Typically, adequatelevels are achieved by allowing CHG to dry com-

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pletely. New strategies for preoperative bathing withchlorhexidine, such as preimpregnated cloths, haveshown promise,175,176 but data are currently insuf-ficient to support this approach.

2. Preoperative intranasal and pharyngeal chlorhexidinetreatment for patients undergoing cardiothoracicprocedures.a. Although data from a randomized controlled trial exist

to support the use of chlorhexidine nasal cream com-bined with 0.12% chlorhexidine gluconate mouth-wash,177 chlorhexidine nasal cream is neither approvedby the Food and Drug Administration (FDA) nor com-mercially available in the United States.

3. Use of gentamicin-collagen sponges.a. Gentamicin-collagen sponges have been evaluated as

a way to decrease SSI among colorectal and cardiacsurgical patients.i. Colorectal surgical patients. Several single-center

randomized trials have demonstrated that genta-micin-collagen sponges decrease the risk of SSI fol-lowing colorectal procedures.178-180 The rate of SSIwas higher with the sponge, however, in a recentlarge, multicenter randomized clinical trial.181

ii. Cardiothoracic surgical patients. Four randomizedcontrolled trials have evaluated the use of genta-micin-collagen sponges in cardiothoracic surgery.Three of these trials demonstrated a decrease inSSIs,182-184 and one showed no difference.185 A recentmeta-analysis combining these trials concluded thatthe risk of deep sternal wound infection was sig-nificantly lower in patients who received a genta-micin-collagen sponge than in patients who did not(RR, 0.62 [95% CI, 0.39–0.97]) despite significantheterogeneity among the trials.186

b. Gentamicin-collagen sponges are not currently ap-proved by the FDA for use in the United States.

4. Use of bundles to ensure compliance with best practices.a. Bundles have been promoted as methods to improve

adherence to best practices.b. Although generally favorable, the use of bundles for

the prevention of SSI has led to mixed results, de-pending on which components are included.59,187,188

c. Thus, there is no consensus on the components ofan effective bundle to prevent SSIs.

section 5: performance measures

I. Internal reportingThese performance measures are intended to support

internal hospital quality improvement efforts and do notnecessarily address external reporting needs. The processand outcome measures suggested here are derived frompublished guidelines, other relevant literature, and theopinion of the authors. Report process and outcome mea-

sures to senior hospital leadership, nursing leadership, andclinicians who care for patients at risk for SSI.A. Process measures

1. Compliance with antimicrobial prophylaxis guide-lines.a. Measure the percentage of procedures in which an-

timicrobial prophylaxis was appropriately pro-vided. Appropriateness includes (1) correct type ofagent, (2) start of administration of the agentwithin 1 hour of incision (2 hours allowed for van-comycin and fluoroquinolones), and (3) discon-tinuation of the agent within 24 hours after surgery.i. Numerator: number of patients who appropri-

ately received antimicrobial prophylaxis.ii. Denominator: total number of selected opera-

tions performed.iii. Multiply by 100 so that the measure is expressed

as a percentage.2. Compliance with hair removal guidelines.

a. Measure the percentage of procedures for whichhair removal is appropriately performed (ie, clip-ping, use of a depilatory or no hair removal isperformed rather than use of razor).i. Numerator: number of patients with appropri-

ate perioperative hair removal.ii. Denominator: total number of selected opera-

tions performed.iii. Multiply by 100 so that the measure is expressed

as a percentage.3. Compliance with perioperative glucose control

guidelines.a. Measure the percentage of procedures for which

serum glucose is 180 mg/dL or lower within 18–24 hours after anesthesia end time for all cardiacsurgery patients.60,61,100

i. Numerator: number of patients with appropri-ately maintained serum glucose (180 mg/dL orlower) in the time frame of 18–24 hours afteranesthesia end time following cardiac surgery.

ii. Denominator: total number of cardiac proce-dures performed.

iii. Multiply by 100 so that the measure is expressedas a percentage.

B. Outcome measures1. SSI rate

a. Use NHSN definitions and risk adjustment meth-ods for SSI (available at http://www.cdc.gov/nhsn/acute-care-hospital/ssi/index.html).i. Numerator: number of patients with an SSI fol-

lowing selected operations.ii. Denominator: total number of selected opera-

tions performed.iii. Multiply by 100 so that the measure is expressed

as the number of SSIs per 100 procedures.

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iv. Rates of SSI can be risk adjusted using one of2 methods: stratification using the NHSN riskindex133 or calculation of the standardized in-fection ratio (SIR).189 NHSN now promotes theuse of SIR over the NHSN risk index for im-proved risk adjustment potential,190 and SIR ispreferentially used for the national public re-porting outcome measure within NHSN.

(a) The NHSN risk index is an operation- andpatient-specific prospectively applied riskscore that predicts SSIs.191 This risk indexincludes 3 predictors of increased risk of SSI:(1) estimators of wound microbial contam-ination, (2) duration of operation, and (3)markers for host susceptibility.42

(b) SIR is the ratio of the observed number ofSSIs (O) that occurred compared with theexpected number for a surgeon performinga specific type of procedure (E ; eg, SIR pO/E).189 The expected number of SSIs canbe obtained by multiplying the number ofoperations done by the surgeon in each pro-cedure risk category by the NHSN rate forthe same procedure risk category and divid-ing by 100. Values that exceed 1.0 indicatethat more SSIs occurred than expected. Im-portantly, SIR can only be calculated if thenumber of expected HAIs is ≥1. Thus, thisapproach may be more difficult for smallsurgical programs or if few procedures areperformed for any one procedure type.192

(c) Risk adjustment using logistic regression andthe SIR method generally provides better risk-adjustment than the basic risk index.190,193

II. External reportingThere are many challenges in providing useful infor-

mation to consumers and other stakeholders while pre-venting unintended adverse consequences of public re-porting of HAIs.194 Recommendations and requirementsfor public reporting of HAIs have been provided byHICPAC,195 the Healthcare-Associated Infection WorkingGroup of the Joint Public Policy Committee,54 the Na-tional Quality Forum,55 and CMS.196 The following is anexample of an external performance measure that is cur-rently required by some healthcare stakeholders andregulators.

A. Process measures1. Compliance with CMS antimicrobial prophylaxis

guidelines (see the section above on internal reportingin “Section 5: Performance Measures”).a. Measure the percentage of procedures in which an-

timicrobial prophylaxis was appropriately pro-vided. Appropriateness includes correct type ofagent, administration of the agent within 1 hour

of incision (2 hours are allowed for vancomycinand fluoroquinolones), and discontinuation of theagent within 24 hours after surgery (48 hours forcardiothoracic procedures).197

2. Compliance with the CMS guideline for control ofpostoperative blood glucose in cardiac surgerypatients.a. Measure the percentage of procedures in which

postoperative blood glucose was appropriately con-trolled in cardiac surgery patients.

B. Federal and state requirements1. Federal requirements

a. The CMS published a final rule in the Federal Reg-ister on August 18, 2011, that includes SSI reportingvia the CDC’s NHSN in the CMS Hospital IQRprogram requirements for 2012.196 More specifi-cally, the rule announced a reporting requirementfor SSI data for inpatient abdominal hysterectomyand inpatient colon procedures beginning with sur-gical procedures performed on January 1, 2012.198

b. The requirements for SSI reporting to NHSN forthe IQR program do not preempt or supersedestate mandates for SSI reporting to NHSN (ie, hos-pitals in states with an SSI reporting mandate mustabide by their state’s requirements, even if they aremore extensive than the requirements for this CMSprogram). NHSN users reporting SSI data to thesystem must adhere to the definitions and report-ing requirements for SSIs as specified in the NHSNPatient Safety Component Protocol Manual.198 Formore information, see http://www.cdc.gov/nhsn/acute-care-hospital/ssi/index.html.

2. State requirements and collaborativesa. State requirements. Hospitals in states that have

mandatory SSI reporting requirements must collectand report the data required by the state. For in-formation on state requirements, check with yourstate or local health department.

b. State collaboratives. Currently 27 states have im-plemented voluntary SSI collaboratives. For moreinformation on state collaboratives for SSI, seehttp://www.cdc.gov/hai/stateplans/states-w-SSI-collaborative.html.

3. External quality initiativesa. Several external quality initiatives focused on SSI

prevention are ongoing. The benefits in partici-pation in these external quality initiatives is un-known but may include improvement in the cul-ture of safety and patient outcomes, includingdecreased rates of SSI. For additional information,see the following:i. http://www.ahrq.gov/qual/haify11.htm#projects

ii. http://www.ihi.org/Engage/Initiatives/Completed/ProjectJOINTS/Pages/default.aspx

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table 3. Fundamental Elements of Accountability for Healthcare-Associated Infection Prevention

Senior management is responsible for ensuring that the healthcare system supports an infection prevention and control (IPC) pro-gram that effectively prevents healthcare-associated infections (HAIs) and the transmission of epidemiologically importantpathogens

Senior management is accountable for ensuring that an adequate number of trained personnel are assigned to the IPC program andadequate staffing of other departments that play a key role in HAI prevention (eg, environmental services)

Senior management is accountable for ensuring that healthcare personnel, including licensed and nonlicensed personnel, are ade-quately trained and competent to perform their job responsibilities

Direct healthcare providers (such as physicians, nurses, aides, and therapists) and ancillary personnel (such as environmental serviceand equipment processing personnel) are responsible for ensuring that appropriate IPC practices are used at all times (includinghand hygiene, standard and isolation precautions, and cleaning and disinfection of equipment and the environment)

Senior and unit leaders are responsible for holding personnel accountable for their actionsIPC leadership is responsible for ensuring that an active program to identify HAIs is implemented, that HAI data are analyzed and

regularly provided to those who can use the information to improve the quality of care (eg, unit staff, clinicians, and hospitaladministrators), and that evidence-based practices are incorporated into the program

Senior and unit leaders are accountable for ensuring that appropriate training and educational programs to prevent HAIs are devel-oped and provided to personnel, patients, and families

Personnel from the IPC program, the laboratory, and information technology departments are responsible for ensuring that systemsare in place to support the surveillance program

section 6: examples ofimplementation strategies

Accountability is an essential principle for preventing HAIs.It provides the necessary translational link between scienceand implementation. Without clear accountability, scientifi-cally based implementation strategies will be used in an in-consistent and fragmented way, decreasing their effectivenessin preventing HAIs. Accountability begins with the chief ex-ecutive officer and other senior leaders who provide the im-perative for HAI prevention, thereby making HAI preventionan organizational priority. Senior leadership is accountablefor providing adequate resources needed for effective imple-mentation of an HAI prevention program. These resourcesinclude necessary personnel (clinical and nonclinical), edu-cation, and equipment (Table 3).

The following information identifies implementation strat-egies that can be used as part of a program to prevent andreduce the risk for SSI. The implementation strategies areorganized under 4 concepts: engage, educate, execute, andevaluate.199

I. EngageIn the engagement phase, there needs to be clear and

effective communication pertaining to the reasons why theSSI implementation strategies are important for patientcare. Engagement of senior leadership, physician cham-pions, infection preventionists, and multidisciplinaryteams are examples of strategies necessary for initial im-plementation of a program to reduce SSIs. The followingimplementation strategies are described in the literature asbeing essential for the engagement process.A. Obtaining support for SSI reduction from senior leader-

ship. Senior leadership support is an important factorcontributing to SSI rate decreases. Senior leadership isalso critical for sustaining improvements over time.

Senior leadership can include but is not limited to thehospital’s board, president, chief operating officer, chiefmedical officer, and chief nursing officer.148,200-203

B. Obtaining highly engaged physicians as champions. Med-ical and surgical staff engagement is critical for SSI pre-vention activities and to champion SSI preventionthroughout the hospital. Examples include a physicianleading an SSI prevention multidisciplinary team anda physician champion who provides education on strat-egies to reduce SSIs to other physicians and staff.202,203

C. Use of multidisciplinary teams. Numerous studies andliterature address the effectiveness of multidisciplinaryteams to plan, develop, implement, and evaluate effortsto reduce SSIs. The key components of the team includepreoperative, intraoperative, and postoperative man-agement of the patient. Teams should include nursing,pharmacy, and physician champions.148,200,204-207

D. Adopting evidence-based practices and guidelines. Severalstudies in the literature focus on the need for hospitalsto adopt evidence-based practices and guidelines in aneffort to decrease the risk of SSIs. The literature stressesthat, although evidence-based interventions can reducethe number of SSIs and improve patient outcomes,implementation of these practices nationally occurs lessfrequently than is desirable.10,148,203,208-210

E. Focus on a culture of safety. The literature supports theneed for a culture of safety to successfully implementa program focusing on reducing SSIs. A culture of safetyfocuses on teamwork, technical processes, and pro-moting accountability for preventing SSIs throughoutthe continuum of care.136,200,202

II. EducateEducation pertaining to practices to prevent SSIs is es-

sential for senior leadership, physicians, nurses, and pa-tients and families. The following implementation strat-

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egies describe the types of education that can impact SSIrates and who should be the focus of educational efforts.

A. Aligned and coordinated SSI education for licensed in-dependent practitioners and staff. Multidisciplinary ed-ucation for licensed independent practitioners (physi-cians and midlevel practitioners) and other practitionerstaff (registered nurses) must be aligned and coordi-nated. The content of the education focuses on thecontinuum of the patient’s care and execution of evi-dence-based practices to prevent SSIs.202,203

B. One-to-one education of the surgeon when an SSI issueis identified. Provide one-to-one education when sur-geons have elevated SSI rates and/or when appropriatepreventive processes are not being adhered to. This ed-ucation may be conducted by another surgeon, infec-tion preventionist, quality office, or other qualified in-dividuals. The education should be nonconfrontationalwith an emphasis on understanding variation in prac-tice rather than judgment. If lack of adherence to evi-dence-based practices is identified, then an action planmust be developed.203

C. Education for senior leadership that describes the valueand benefits of SSI reduction. Provide education to ex-ecutive leadership regarding the value of reducing SSIs,including patient and fiscal outcomes.131

D. Education for the surgical team on safety science. Provideeducation to licensed independent practitioners andstaff involved in the care of surgical patients on thescience of safety, including the principles of safe systemdesign.200

E. Specific SSI education for patients and families. Patienteducation for reducing SSIs is a major priority for anyhospital focused on preventing SSIs. Education strate-gies such as presurgical classes, television education, andone-to-one education with the patient and family havebeen used successfully. Educational materials should beprovided in multiple languages on the basis of the pop-ulation served.131,202,203

III. ExecuteIn the execution phase, the focus is on implementation

strategies to reduce barriers and improve adherence withevidence-based practices and reduce the risk of SSIs, in-cluding (a) standardization of care processes, (b) creatingredundancy or independent checks, and (c) learning fromdefects when an SSI occurs. As noted above, no consensusexists on the components of an effective bundle to pre-vent SSIs. Thus, individual hospitals must identify localdeficits and create their own bundle.

A. Use a quality improvement methodology. Use of qualityimprovement methodology for designing and imple-menting a program leads to reduced rates of SSIs. Qual-ity improvement methodologies include Lean SixSigma, the Comprehensive Unit-Based Safety Program,and the Plan-Do-Check-Act model. Various perfor-mance improvement (PI) tools have been used, in-

cluding dashboards, scorecards, and histograms, to dis-play data.149,200,203,207,211

B. Differentiate between adult and pediatric populations.Pediatric-focused evidence-based practices for reducingSSIs are lacking. Clinical interventions designed for theadult population cannot necessarily be transferred tothe pediatric population. Hospital and pediatric sur-geons must determine whether adult evidence-basedinterventions can be safely used with the pediatricpopulation.203

C. Use of information technologies (IT). IT innovations canbe used to simplify and standardize clinical documen-tation. IT and the electronic medical record can alsobe used for electronic surveillance, electronic prompts,automatic stops for prophylactic antibiotic orders, andeducation. Education can be delivered to patients, fam-ilies, and healthcare workers through different media,including the Internet and television.148,202,203,212

D. Participation in a collaborative. Numerous studies havereported that participation in a collaborative can helpreduce SSI rates in participating organizations. Colla-boratives provide a mechanism for organizations to

1. Utilize valid data, such as with the American Collegeof Surgeons National Surgical Quality ImprovementProgram;213

2. Identify increased morbidity and mortality throughcomparisons to peer hospitals on a national basis;213

and3. Learn through the collaboration pro-

cess.161,202,203,205,207,209,213,214

E. Use of preoperative/postoperative order sets. Standardizedorder sets can be developed on the basis of evidence-based practices. The order sets should be approved bythe medical staff and updated when the evidence-basedpractices change. The development of order sets is alabor-intensive process necessitating skills and expertiseof several disciplines, including surgery, anesthesia,nursing, and pharmacy. All relevant disciplines shouldbe educated in the use of the order sets.148,202,203

F. Acting on identified SSI issues. When issues suspected ofincreasing the risk of SSI are identified, the hospitalshould take action to resolve the identified issues. Sev-eral hospitals conduct root-cause analyses with a mul-tidisciplinary team to identify the cause of the issuesand any lack of adherence in the evidence-based prac-tices.149,202-204

G. Establish a protocol for preoperative testing. Establish aprotocol for procedure-specific preoperative testing todetect medical conditions that increase the risk of SSI.The protocol should focus on nutritional counseling ifindicated, smoking cessation if indicated, preadmissioninfections, and reconciling medications with adjust-ments prior to surgery if indicated.202 If high-risk pa-tients are identified through screening, alerts should beadded to electronic medical records to ensure that all

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members of the perioperative team are aware of thehigh-risk condition(s).

IV. EvaluateIn the evaluation phase, the focus is on the use of

measurement and evaluation tools to determine the ef-fectiveness of implementation strategies in the preventionof SSIs.

A. Use of performance improvement tools. Various PI toolscan be used. PI tools include dashboards, scorecards,or histograms to display data. Additional PI tools caninclude root-cause analysis and failure modes and ef-fects analysis.148,202,203

B. Direct observation of evidence-based practices. As part ofa hospital’s SSI improvement activities, trained observ-ers (eg, infection preventionists, educators, nurses, andphysicians) should observe surgery to assure that evi-dence-based practices have been implemented in theoperating room. Direct observation can also be con-ducted for hand hygiene and surgical hand antisepsistechnique. This activity is used to educate and reinforceevidence-based practices with the operating roompractitioners.136,149,203,214

C. Longitudinal evaluation of SSI rates and compliance rates.Track the success of the SSI reduction program by eval-uating SSI rates over time (ie, before, during, and afterthe program). If specific practices or processes are iden-tified for improvement, evaluate the compliance withevidence-based practices related to these practices andprocesses. Feed these data evaluations back to frontlinestaff.

acknowledgments

Disclaimer. S.I.B.-T.—The findings and conclusions in this report are thoseof the authors and do not necessarily represent the official position of theCenters for Disease Control and Prevention.

Potential conflicts of interest. E.P.D. reports serving as an advisor/con-sultant for Merck, Baxter, Ortho-McNeil, Targanta, Rib-X, Affinium, 3M,Schering-Plough, Astellas, CareFusion, Durata, Pfizer, and Applied Medicaland receiving grant support from Tetraphase. L.G. reports receiving honorariafrom Premier, CareFusion, and Infection Control Today. K.S.K. reports re-ceiving grant support and serving as an advisor/consultant for Sage Products.D.J.A., K.P., D.W.B., S.I.B.-T., A.-C.N., L.L.M., L.S., and D.S.Y. report norelevant conflicts of interest.

Address correspondence to Deverick J. Anderson, MD, MPH, Division ofInfectious Diseases, Box 102359, Duke University Medical Center, Durham,NC 27710 ([email protected]).

references

1. Anderson DJ, Kaye KS, Classen D, et al. Strategies to preventsurgical site infections in acute care hospitals. Infect ControlHosp Epidemiol 2008;29(suppl 1):S51–S61.

2. Yokoe DS, Anderson DJ, Berenholtz SM, et al. Introduction to“A Compendium of Strategies to Prevent Healthcare-Associ-

ated Infections in Acute Care Hospitals: 2014 Updates.” InfectControl Hosp Epidemiol 2014;35(5):455–459.

3. Cruse P. Wound infection surveillance. Rev Infect Dis 1981;3(4):734–737.

4. Graves EJ. National Hospital Discharge Survey: Annual Sum-mary, 1987. Series 13, no. 99. Hyattsville, MD: National Centerfor Health Statistics, 1989.

5. Agency for Healthcare Research and Quality. Healthcare Costand Utilization Project—statistics on hospital stays. 2013.http://hcupnet.ahrq.gov/. Accessed February 15, 2013.

6. Scott RD. The Direct Medical Costs of Healthcare-AssociatedInfections in U.S. Hospitals and the Benefits of Prevention. At-lanta: Centers for Disease Control and Prevention, 2009.http://www.cdc.gov/hai/pdfs/hai/scott_costpaper.pdf. Ac-cessed December 14, 2013.

7. Anderson DJ, Pyatt DG, Weber DJ, Rutala WA. Statewide costsof health care–associated infections: estimates for acute carehospitals in North Carolina. Am J Infect Control 2013;41(9):764–768.

8. Lewis SS, Moehring RW, Chen LF, Sexton DJ, Anderson DJ.Assessing the relative burden of hospital-acquired infections ina network of community hospitals. Infect Control Hosp Epi-demiol 2013;34(11):1229–1230.

9. Zimlichman E, Henderson D, Tamir O, et al. Health care–associated infections: a meta-analysis of costs and financialimpact on the us health care system. JAMA Intern Med 2013;173(22):2039–2046.

10. Meeks DW, Lally KP, Carrick MM, et al. Compliance withguidelines to prevent surgical site infections: as simple as1-2-3? Am J Surg 2011;201(1):76–83.

11. Umscheid CA, Mitchell MD, Doshi JA, Agarwal R, WilliamsK, Brennan PJ. Estimating the proportion of healthcare-asso-ciated infections that are reasonably preventable and the relatedmortality and costs. Infect Control Hosp Epidemiol 2011;32(2):101–114.

12. Klevens RM, Edwards JR, Richards CL Jr, et al. Estimatinghealth care–associated infections and deaths in U.S. hospitals,2002. Public Health Rep 2007;122(2):160–166.

13. Cruse PJ, Foord R. The epidemiology of wound infection: a10-year prospective study of 62,939 wounds. Surg Clin NorthAm 1980;60(1):27–40.

14. Anderson DJ, Kaye KS, Chen LF, et al. Clinical and financialoutcomes due to methicillin resistant Staphylococcus aureus sur-gical site infection: a multi-center matched outcomes study.PloS ONE 2009;4(12):e8305.

15. Engemann JJ, Carmeli Y, Cosgrove SE, et al. Adverse clinicaland economic outcomes attributable to methicillin resistanceamong patients with Staphylococcus aureus surgical site infec-tion. Clin Infect Dis 2003;36(5):592–598.

16. Kirkland KB, Briggs JP, Trivette SL, Wilkinson WE, Sexton DJ.The impact of surgical-site infections in the 1990s: attributablemortality, excess length of hospitalization, and extra costs. In-fect Control Hosp Epidemiol 1999;20(11):725–730.

17. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR;Hospital Infection Control Practices Advisory Committee.Guideline for prevention of surgical site infection, 1999. InfectControl Hosp Epidemiol 1999;20(4):250–278.

18. Apisarnthanarak A, Jones M, Waterman BM, Carroll CM, Ber-nardi R, Fraser VJ. Risk factors for spinal surgical-site infections

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 18: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

strategies to prevent ssi: 2014 update 621

in a community hospital: a case-control study. Infect ControlHosp Epidemiol 2003;24(1):31–36.

19. Boyce JM, Potter-Bynoe G, Dziobek L. Hospital reimbursementpatterns among patients with surgical wound infections fol-lowing open heart surgery. Infect Control Hosp Epidemiol 1990;11(2):89–93.

20. Coello R, Glenister H, Fereres J, et al. The cost of infection insurgical patients: a case-control study. J Hosp Infect 1993;25(4):239–250.

21. Hollenbeak CS, Murphy DM, Koenig S, Woodward RS, Dun-agan WC, Fraser VJ. The clinical and economic impact of deepchest surgical site infections following coronary artery bypassgraft surgery. Chest 2000;118(2):397–402.

22. VandenBergh MF, Kluytmans JA, van Hout BA, et al. Cost-effectiveness of perioperative mupirocin nasal ointment in car-diothoracic surgery. Infect Control Hosp Epidemiol 1996;17(12):786–792.

23. Vegas AA, Jodra VM, Garcia ML. Nosocomial infection in sur-gery wards: a controlled study of increased duration of hospitalstays and direct cost of hospitalization. Eur J Epidemiol 1993;9(5):504–510.

24. Whitehouse JD, Friedman ND, Kirkland KB, Richardson WJ,Sexton DJ. The impact of surgical-site infections following or-thopedic surgery at a community hospital and a universityhospital: adverse quality of life, excess length of stay, and extracost. Infect Control Hosp Epidemiol 2002;23(4):183–189.

25. Bozic KJ, Katz P, Cisternas M, Ono L, Ries MD, Showstack J.Hospital resource utilization for primary and revision total hiparthroplasty. J Bone Joint Surg Am 2005;87(3):570–576.

26. National Healthcare Safety Network. Surgical Site Infection (SSI)Event. Atlanta: Centers for Disease Control and Prevention, 2013.http://www.cdc.gov/nhsn/PDFs/pscManual/9pscSSIcurrent.pdf.Accessed May 1, 2013.

27. Condon RE, Schulte WJ, Malangoni MA, Anderson-Teschen-dorf MJ. Effectiveness of a surgical wound surveillance pro-gram. Arch Surg 1983;118(3):303–307.

28. Kerstein M, Flower M, Harkavy LM, Gross PA. Surveillancefor postoperative wound infections: practical aspects. Am Surg1978;44(4):210–214.

29. Mead PB, Pories SE, Hall P, Vacek PM, Davis JH Jr, GamelliRL. Decreasing the incidence of surgical wound infections: val-idation of a surveillance-notification program. Arch Surg 1986;121(4):458–461.

30. Baker C, Luce J, Chenoweth C, Friedman C. Comparison ofcase-finding methodologies for endometritis after cesarean sec-tion. Am J Infect Control 1995;23(1):27–33.

31. Cardo DM, Falk PS, Mayhall CG. Validation of surgical woundsurveillance. Infect Control Hosp Epidemiol 1993;14(4):211–215.

32. Ming DY, Chen LF, Miller BA, Anderson DJ. The impact ofdepth of infection and postdischarge surveillance on rate ofsurgical-site infections in a network of community hospitals.Infect Control Hosp Epidemiol 2012;33(3):276–282.

33. Chalfine A, Cauet D, Lin WC, et al. Highly sensitive and ef-ficient computer-assisted system for routine surveillance forsurgical site infection. Infect Control Hosp Epidemiol 2006;27(8):794–801.

34. Miner AL, Sands KE, Yokoe DS, et al. Enhanced identificationof postoperative infections among outpatients. Emerg Infect Dis2004;10(11):1931–1937.

35. Yokoe DS, Noskin GA, Cunnigham SM, et al. Enhanced iden-

tification of postoperative infections among inpatients. EmergInfect Dis 2004;10(11):1924–1930.

36. Calderwood MS, Kleinman K, Bratzler DW, et al. Use of Med-icare claims to identify US hospitals with a high rate of surgicalsite infection after hip arthroplasty. Infect Control Hosp Epi-demiol 2013;34(1):31–39.

37. Huang SS, Placzek H, Livingston J, et al. Use of Medicare claimsto rank hospitals by surgical site infection risk following cor-onary artery bypass graft surgery. Infect Control Hosp Epidemiol2011;32(8):775–783.

38. Haley VB, Van Antwerpen C, Tserenpuntsag B, et al. Use ofadministrative data in efficient auditing of hospital-acquiredsurgical site infections, New York State 2009–2010. Infect Con-trol Hosp Epidemiol 2012;33(6):565–571.

39. Burke JP. Infection control—a problem for patient safety. NEngl J Med 2003;348(7):651–656.

40. Cullen KA, Hall MJ, Golosinkiy A. Ambulatory surgery in theUnited States, 2006. Natl Health Stat Report 2009;(11):1–25.

41. National action plan to prevent health care–associated infec-tions: roadmap to elimination; ambulatory surgical centers.Department of Health and Human Services website. http://www.hhs.gov/ash/initiatives/hai/ambulatory_surgical_centers.html. Accessed January 4, 2013.

42. Consensus paper on the surveillance of surgical wound infec-tions. The Society for Hospital Epidemiology of America; theAssociation for Practitioners in Infection Control; the Centersfor Disease Control; the Surgical Infection Society. Infect Con-trol Hosp Epidemiol 1992;13(10):599–605.

43. Mannien J, Wille JC, Snoeren RL, van den Hof S. Impact ofpostdischarge surveillance on surgical site infection rates forseveral surgical procedures: results from the nosocomial sur-veillance network in the Netherlands. Infect Control Hosp Ep-idemiol 2006;27(8):809–816.

44. Kent P, McDonald M, Harris O, Mason T, Spelman D. Post-discharge surgical wound infection surveillance in a provincialhospital: follow-up rates, validity of data and review of theliterature. ANZ J Surg 2001;71(10):583–589.

45. Manian FA. Surveillance of surgical site infections in alternativesettings: exploring the current options. Am J Infect Control1997;25(2):102–105.

46. Michelson J. Improved detection of orthopaedic surgical siteinfections occurring in outpatients. Clin Orthop Relat Res2005(433):218–224.

47. Nafziger DA, Lundstrom T, Chandra S, Massanari RM. Infec-tion control in ambulatory care. Infect Dis Clin North Am 1997;11(2):279–296.

48. Petherick ES, Dalton JE, Moore PJ, Cullum N. Methods foridentifying surgical wound infection after discharge from hos-pital: a systematic review. BMC Infect Dis 2006;6:170.

49. Mlangeni D, Babikir R, Dettenkofer M, Daschner F, GastmeierP, Ruden H. AMBU-KISS: quality control in ambulatory sur-gery. Am J Infect Control 2005;33(1):11–14.

50. Whitby M, McLaws ML, Collopy B, et al. Post-discharge sur-veillance: can patients reliably diagnose surgical wound infec-tions? J Hosp Infect 2002;52(3):155–160.

51. Manian FA, Meyer L. Comparison of patient telephone surveywith traditional surveillance and monthly physician question-naires in monitoring surgical wound infections. Infect ControlHosp Epidemiol 1993;14(4):216–218.

52. Prospero E, Cavicchi A, Bacelli S, Barbadoro P, Tantucci L,

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 19: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

622 infection control and hospital epidemiology june 2014, vol. 35, no. 6

D’Errico MM. Surveillance for surgical site infection after hos-pital discharge: a surgical procedure-specific perspective. InfectControl Hosp Epidemiol 2006;27(12):1313–1317.

53. Sands K, Vineyard G, Platt R. Surgical site infections occurringafter hospital discharge. J Infect Dis 1996;173(4):963–970.

54. Healthcare-Associated Infection Working Group of the JointPublic Policy Committee. Essentials of Public Reporting ofHealthcare-Associated Infections: A Tool Kit. 2007. http://www.shea-online.org/Assets/files/Essentials_of_Public_Reporting_Tool_Kit.pdf. Accessed January 5, 2013.

55. National Quality Forum (NQF). National Voluntary ConsensusStandards for the Reporting of Healthcare-Associated InfectionData. Washington, DC: NQF, 2008. http://www.qualityforum.org/Publications/2008/03/National_Voluntary_Consensus_Standards_for_the_Reporting_of_Healthcare-Associated_Infection_Data.aspx. Accessed January 6, 2013.

56. National Institute for Health and Clinical Excellence (NICE).Surgical Site Infection: Prevention and Treatment of Surgical SiteInfection. London: NICE, 2008. http://www.nice.org.uk/nicemedia/pdf/CG74NICEGuideline.pdf. Accessed February12, 2013.

57. Bratzler DW, Houck PM. Antimicrobial prophylaxis for sur-gery: an advisory statement from the National Surgical Infec-tion Prevention Project. Clin Infect Dis 2004;38(12):1706–1715.

58. Bratzler DW, Hunt DR. The surgical infection prevention andsurgical care improvement projects: national initiatives to im-prove outcomes for patients having surgery. Clin Infect Dis2006;43(3):322–330.

59. Dellinger EP, Hausmann SM, Bratzler DW, et al. Hospitalscollaborate to decrease surgical site infections. Am J Surg 2005;190(1):9–15.

60. National Quality Forum (NQF). Cardiac Surgery Patients withControlled Postoperative Blood Glucose. Washington, DC: NQF,2013. http://www.qualityforum.org/. Accessed January 6, 2013.

61. Lazar HL, McDonnell M, Chipkin SR, et al. The Society ofThoracic Surgeons practice guideline series: blood glucosemanagement during adult cardiac surgery. Ann Thorac Surg2009;87(2):663–669.

62. A resource from the Institute of Healthcare Improvement. In-stitute for Healthcare Improvement (IHI) website. http://www.ihi.org. Accessed January 31, 2007.

63. Griffin FA. Reducing surgical complications. Jt Comm J QualPatient Saf 2007;33(11):660–665.

64. The Joint Commission. National Patient Safety Goals EffectiveJanuary 1, 2013. Oakbrook Terrace, IL: The Joint Commis-sion, 2013. http://www.jointcommission.org/assets/1/18/NPSG_Chapter_Jan2013_HAP.pdf. Accessed March 1, 2013.

65. Centers for Medicare & Medicaid Services. Medicare program;hospital inpatient prospective payment systems for acute carehospitals and the long-term care hospital prospective paymentsystem and fiscal year 2013 rates; hospitals’ resident caps forgraduate medical education payment purposes; quality re-porting requirements for specific providers and for ambulatorysurgical centers. Final rule. Fed Regist 2012;77(170):53257–53750.

66. Centers for Medicare & Medicaid Services. Medicare program;hospital inpatient value-based purchasing program. Final rule.Fed Regist 2011;76(88):26490–26547.

67. van Kasteren ME, Mannien J, Kullberg BJ, et al. Quality im-provement of surgical prophylaxis in Dutch hospitals: evalu-

ation of a multi-site intervention by time series analysis. JAntimicrob Chemother 2005;56(6):1094–1102.

68. Schweon S. Stamping out surgical site infections. RN 2006;69(8):36–40.

69. Torpy JM, Burke A, Glass RM. JAMA patient page: woundinfections. JAMA 2005;294(16):2122.

70. Kanter G, Connelly NR, Fitzgerald J. A system and processredesign to improve perioperative antibiotic administration.Anesth Analg 2006;103(6):1517–1521.

71. Pestotnik SL, Classen DC, Evans RS, Burke JP. Implementingantibiotic practice guidelines through computer-assisted de-cision support: clinical and financial outcomes. Ann Intern Med1996;124(10):884–890.

72. Webb AL, Flagg RL, Fink AS. Reducing surgical site infectionsthrough a multidisciplinary computerized process for preop-erative prophylactic antibiotic administration. Am J Surg 2006;192(5):663–668.

73. Nair BG, Newman SF, Peterson GN, Wu WY, Schwid HA.Feedback mechanisms including real-time electronic alerts toachieve near 100% timely prophylactic antibiotic administra-tion in surgical cases. Anesth Analg 2010;111(5):1293–1300.

74. Berger RG, Kichak JP. Computerized physician order entry:helpful or harmful? J Am Med Inform Assoc 2004;11(2):100–103.

75. Antimicrobial prophylaxis for surgery. Treat Guidel Med Lett2009;7(82):47–52.

76. Bratzler DW, Dellinger EP, Olsen KM, et al. Clinical practiceguidelines for antimicrobial prophylaxis in surgery. Am J HealthSyst Pharm 2013;70(3):195–283.

77. Steinberg JP, Braun BI, Hellinger WC, et al. Timing of anti-microbial prophylaxis and the risk of surgical site infections:results from the Trial to Reduce Antimicrobial Prophylaxis Er-rors. Ann Surg 2009;250(1):10–16.

78. van Kasteren ME, Mannien J, Ott A, Kullberg BJ, de Boer AS,Gyssens IC. Antibiotic prophylaxis and the risk of surgical siteinfections following total hip arthroplasty: timely administra-tion is the most important factor. Clin Infect Dis 2007;44(7):921–927.

79. Soriano A, Bori G, Garcia-Ramiro S, et al. Timing of antibioticprophylaxis for primary total knee arthroplasty performed dur-ing ischemia. Clin Infect Dis 2008;46(7):1009–1014.

80. Akinyoola AL, Adegbehingbe OO, Odunsi A. Timing of an-tibiotic prophylaxis in tourniquet surgery. J Foot Ankle Surg2011;50(4):374–376.

81. Harbarth S, Samore MH, Lichtenberg D, Carmeli Y. Prolongedantibiotic prophylaxis after cardiovascular surgery and its effecton surgical site infections and antimicrobial resistance. Cir-culation 2000;101(25):2916–2921.

82. McDonald M, Grabsch E, Marshall C, Forbes A. Single- versusmultiple-dose antimicrobial prophylaxis for major surgery: asystematic review. Aust N Z J Surg 1998;68(6):388–396.

83. Coakley BA, Sussman ES, Wolfson TS, et al. Postoperative an-tibiotics correlate with worse outcomes after appendectomy fornonperforated appendicitis. J Am Coll Surg 2011;213(6):778–783.

84. Cannon JA, Altom LK, Deierhoi RJ, et al. Preoperative oralantibiotics reduce surgical site infection following elective co-lorectal resections. Dis Colon Rectum 2012;55(11):1160–1166.

85. Englesbe MJ, Brooks L, Kubus J, et al. A statewide assessment

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 20: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

strategies to prevent ssi: 2014 update 623

of surgical site infection following colectomy: the role of oralantibiotics. Ann Surg 2010;252(3):514–519.

86. Fry DE. Colon preparation and surgical site infection. Am JSurg 2011;202(2):225–232.

87. Hendren S, Fritze D, Banerjee M, et al. Antibiotic choice isindependently associated with risk of surgical site infectionafter colectomy: a population-based cohort study. Ann Surg2013;257(3):469–475.

88. Lewis RT. Oral versus systemic antibiotic prophylaxis in electivecolon surgery: a randomized study and meta-analysis send amessage from the 1990s. Can J Surg 2002;45(3):173–180.

89. Nelson RL, Glenny AM, Song F. Antimicrobial prophylaxis forcolorectal surgery. Cochrane Database Syst Rev 2009;(1):CD001181.

90. Deierhoi RJ, Dawes LG, Vick C, Itani KM, Hawn MT. Choiceof intravenous antibiotic prophylaxis for colorectal surgerydoes matter. J Am Coll Surg 2013;217(5):763–769.

91. Toneva GD, Deierhoi RJ, Morris M, et al. Oral antibiotic bowelpreparation reduces length of stay and readmissions after co-lorectal surgery. J Am Coll Surg 2013;216(4):756–762.

92. Guenaga KF, Matos D, Wille-Jorgensen P. Mechanical bowelpreparation for elective colorectal surgery. Cochrane DatabaseSyst Rev 2011;(9):CD001544.

93. Tanner J, Woodings D, Moncaster K. Preoperative hair removalto reduce surgical site infection. Cochrane Database Syst Rev2006;(3):CD004122.

94. Dronge AS, Perkal MF, Kancir S, Concato J, Aslan M, RosenthalRA. Long-term glycemic control and postoperative infectiouscomplications. Arch Surg 2006;141(4):375–380.

95. Golden SH, Peart-Vigilance C, Kao WH, Brancati FL. Periop-erative glycemic control and the risk of infectious complica-tions in a cohort of adults with diabetes. Diabetes Care 1999;22(9):1408–1414.

96. Olsen MA, Nepple JJ, Riew KD, et al. Risk factors for surgicalsite infection following orthopaedic spinal operations. J BoneJoint Surg Am 2008;90(1):62–69.

97. Kwon S, Thompson R, Dellinger P, Yanez D, Farrohki E, FlumD. Importance of perioperative glycemic control in generalsurgery: a report from the Surgical Care and Outcomes As-sessment Program. Ann Surg 2013;257(1):8–14.

98. Umpierrez GE, Smiley D, Jacobs S, et al. Randomized studyof basal-bolus insulin therapy in the inpatient management ofpatients with type 2 diabetes undergoing general surgery(RABBIT 2 surgery). Diabetes Care 2011;34(2):256–261.

99. Jacobi J, Bircher N, Krinsley J, et al. Guidelines for the use ofan insulin infusion for the management of hyperglycemia incritically ill patients. Crit Care Med 2012;40(12):3251–3276.

100. Umpierrez GE, Hellman R, Korytkowski MT, et al. Manage-ment of hyperglycemia in hospitalized patients in non–criticalcare setting: an endocrine society clinical practice guideline. JClin Endocrinol Metab 2012;97(1):16–38.

101. Gandhi GY, Nuttall GA, Abel MD, et al. Intensive intraoper-ative insulin therapy versus conventional glucose managementduring cardiac surgery: a randomized trial. Ann Intern Med2007;146(4):233–243.

102. Sessler DI. Complications and treatment of mild hypothermia.Anesthesiology 2001;95(2):531–543.

103. Kurz A, Sessler DI, Lenhardt R; Study of Wound Infection andTemperature Group. Perioperative normothermia to reduce the

incidence of surgical-wound infection and shorten hospitali-zation. N Engl J Med 1996;334(19):1209–1215.

104. Melling AC, Ali B, Scott EM, Leaper DJ. Effects of preoperativewarming on the incidence of wound infection after clean sur-gery: a randomised controlled trial. Lancet 2001;358(9285):876–880.

105. Wong PF, Kumar S, Bohra A, Whetter D, Leaper DJ. Random-ized clinical trial of perioperative systemic warming in majorelective abdominal surgery. Br J Surg 2007;94(4):421–426.

106. Belda FJ, Aguilera L, Garcia de la Asuncion J, et al. Supple-mental perioperative oxygen and the risk of surgical woundinfection: a randomized controlled trial. JAMA 2005;294(16):2035–2042.

107. Greif R, Akca O, Horn EP, Kurz A, Sessler DI; Outcomes Re-search Group. Supplemental perioperative oxygen to reducethe incidence of surgical-wound infection. N Engl J Med 2000;342(3):161–167.

108. Bickel A, Gurevits M, Vamos R, Ivry S, Eitan A. Perioperativehyperoxygenation and wound site infection following surgeryfor acute appendicitis: a randomized, prospective, controlledtrial. Arch Surg 2011;146(4):464–470.

109. Meyhoff CS, Wetterslev J, Jorgensen LN, et al. Effect of highperioperative oxygen fraction on surgical site infection andpulmonary complications after abdominal surgery: the PROXIrandomized clinical trial. JAMA 2009;302(14):1543–1550.

110. Pryor KO, Fahey TJ 3rd, Lien CA, Goldstein PA. Surgical siteinfection and the routine use of perioperative hyperoxia in ageneral surgical population: a randomized controlled trial.JAMA 2004;291(1):79–87.

111. Schietroma M, Carlei F, Cecilia EM, Piccione F, Bianchi Z,Amicucci G. Colorectal infraperitoneal anastomosis: the effectsof perioperative supplemental oxygen administration on theanastomotic dehiscence. J Gastrointest Surg 2012;16(2):427–434.

112. Schietroma M, Cecilia EM, Carlei F, et al. Prevention of anas-tomotic leakage after total gastrectomy with perioperative sup-plemental oxygen administration: a prospective randomized,double-blind, controlled, single-center trial. Ann Surg Oncol2013;20(5):1584–1590.

113. Meyhoff CS, Jorgensen LN, Wetterslev J, Christensen KB, Ras-mussen LS. Increased long-term mortality after a high periop-erative inspiratory oxygen fraction during abdominal surgery:follow-up of a randomized clinical trial. Anesth Analg 2012;115(4):849–854.

114. Qadan M, Akca O, Mahid SS, Hornung CA, Polk HC Jr. Peri-operative supplemental oxygen therapy and surgical site in-fection: a meta-analysis of randomized controlled trials. ArchSurg 2009;144(4):359–366.

115. Maiwald M, Chan ES. The forgotten role of alcohol: a system-atic review and meta-analysis of the clinical efficacy and per-ceived role of chlorhexidine in skin antisepsis. PloS ONE 2012;7(9):e44277.

116. Darouiche RO, Wall MJ Jr, Itani KM, et al. Chlorhexidine-alcohol versus povidone-iodine for surgical-site antisepsis. NEngl J Med 2010;362(1):18–26.

117. Swenson BR, Hedrick TL, Metzger R, Bonatti H, Pruett TL,Sawyer RG. Effects of preoperative skin preparation on post-operative wound infection rates: a prospective study of 3 skinpreparation protocols. Infect Control Hosp Epidemiol 2009;30(10):964–971.

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 21: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

624 infection control and hospital epidemiology june 2014, vol. 35, no. 6

118. Aly R, Maibach HI. Comparative antibacterial efficacy of a 2-minute surgical scrub with chlorhexidine gluconate, povidone-iodine, and chloroxylenol sponge-brushes. Am J Infect Control1988;16(4):173–177.

119. Larson E. Guideline for use of topical antimicrobial agents.Am J Infect Control 1988;16(6):253–266.

120. Edwards JP, Ho AL, Tee MC, Dixon E, Ball CG. Wound pro-tectors reduce surgical site infection: a meta-analysis of ran-domized controlled trials. Ann Surg 2012;256(1):53–59.

121. Haynes AB, Weiser TG, Berry WR, et al. A surgical safetychecklist to reduce morbidity and mortality in a global pop-ulation. N Engl J Med 2009;360(5):491–499.

122. Weiser TG, Haynes AB, Dziekan G, Berry WR, Lipsitz SR,Gawande AA. Effect of a 19-item surgical safety checklist duringurgent operations in a global patient population. Ann Surg2010;251(5):976–980.

123. van Klei WA, Hoff RG, van Aarnhem EE, et al. Effects of theintroduction of the WHO “Surgical Safety Checklist” on in-hospital mortality: a cohort study. Ann Surg 2012;255(1):44–49.

124. Haley RW, Culver DH, White JW, et al. The efficacy of infectionsurveillance and control programs in preventing nosocomialinfections in US hospitals. Am J Epidemiol 1985;121(2):182–205.

125. Lee JT. Wound infection surveillance. Infect Dis Clin North Am1992;6(3):643–656.

126. Calderwood MS, Ma A, Khan YM, et al. Use of Medicarediagnosis and procedure codes to improve detection of surgicalsite infections following hip arthroplasty, knee arthroplasty, andvascular surgery. Infect Control Hosp Epidemiol 2012;33(1):40–49.

127. Bolon MK, Hooper D, Stevenson KB, et al. Improved sur-veillance for surgical site infections after orthopedic implan-tation procedures: extending applications for automated data.Clin Infect Dis 2009;48(9):1223–1229.

128. Gerbier-Colomban S, Bourjault M, Cetre JC, Baulieux J, Metz-ger MH. Evaluation study of different strategies for detectingsurgical site infections using the hospital information systemat Lyon University Hospital, France. Ann Surg 2012;255(5):896–900.

129. Yokoe DS, Khan Y, Olsen MA, et al. Enhanced surgical siteinfection surveillance following hysterectomy, vascular, and co-lorectal surgery. Infect Control Hosp Epidemiol 2012;33(8):768–773.

130. Jamtvedt G, Young JM, Kristoffersen DT, O’Brien MA, OxmanAD. Audit and feedback: effects on professional practice andhealth care outcomes. Cochrane Database Syst Rev 2006;(2):CD000259.

131. Skoufalos A, Clarke JL, Napp M, et al. Improving awarenessof best practices to reduce surgical site infection: a multistake-holder approach. Am J Med Qual 2012;27(4):297–304.

132. Association of periOperative Registered Nurses. 2013. http://www.aorn.org/. Accessed March 23, 2013.

133. Culver DH, Horan TC, Gaynes RP, et al; National NosocomialInfections Surveillance System. Surgical wound infection ratesby wound class, operative procedure, and patient risk index.Am J Med 1991;91(3B):152S–157S.

134. Loftus RW, Brown JR, Koff MD, et al. Multiple reservoirs con-tribute to intraoperative bacterial transmission. Anesth Analg2012;114(6):1236–1248.

135. Andersson AE, Bergh I, Karlsson J, Eriksson BI, Nilsson K.Traffic flow in the operating room: an explorative and descrip-tive study on air quality during orthopedic trauma implantsurgery. Am J Infect Control 2012;40(8):750–755.

136. Crolla RM, van der Laan L, Veen EJ, Hendriks Y, van SchendelC, Kluytmans J. Reduction of surgical site infections after im-plementation of a bundle of care. PloS ONE 2012;7(9):e44599.

137. van Rijen M, Bonten M, Wenzel R, Kluytmans J. Mupirocinointment for preventing Staphylococcus aureus infections in na-sal carriers. Cochrane Database Syst Rev 2008;(4):CD006216.

138. Wilcox MH, Hall J, Pike H, et al. Use of perioperative mu-pirocin to prevent methicillin-resistant Staphylococcus aureus(MRSA) orthopaedic surgical site infections. J Hosp Infect 2003;54(3):196–201.

139. Nicholson MR, Huesman LA. Controlling the usage of intra-nasal mupirocin does impact the rate of Staphylococcus aureusdeep sternal wound infections in cardiac surgery patients. AmJ Infect Control 2006;34(1):44–48.

140. Walsh EE, Greene L, Kirshner R. Sustained reduction in meth-icillin-resistant Staphylococcus aureus wound infections aftercardiothoracic surgery. Arch Intern Med 2011;171(1):68–73.

141. Bode LG, Kluytmans JA, Wertheim HF, et al. Preventing sur-gical-site infections in nasal carriers of Staphylococcus aureus.N Engl J Med 2010;362(1):9–17.

142. Harbarth S, Fankhauser C, Schrenzel J, et al. Universal screen-ing for methicillin-resistant Staphylococcus aureus at hospitaladmission and nosocomial infection in surgical patients. JAMA2008;299(10):1149–1157.

143. Perl TM, Cullen JJ, Wenzel RP, et al. Intranasal mupirocin toprevent postoperative Staphylococcus aureus infections. N EnglJ Med 2002;346(24):1871–1877.

144. Schweizer M, Perencevich E, McDanel J, et al. Effectiveness ofa bundled intervention of decolonization and prophylaxis todecrease Gram positive surgical site infections after cardiac ororthopedic surgery: systematic review and meta-analysis. BMJ2013;346:f2743.

145. Miller MA, Dascal A, Portnoy J, Mendelson J. Developmentof mupirocin resistance among methicillin-resistant Staphylo-coccus aureus after widespread use of nasal mupirocin ointment.Infect Control Hosp Epidemiol 1996;17(12):811–813.

146. Whiteside OJ, Tytherleigh MG, Thrush S, Farouk R, GallandRB. Intra-operative peritoneal lavage—who does it and why?Ann R Coll Surg Engl 2005;87(4):255–258.

147. Fournel I, Tiv M, Soulias M, Hua C, Astruc K, Aho Glele LS.Meta-analysis of intraoperative povidone-iodine application toprevent surgical-site infection. Br J Surg 2010;97(11):1603–1613.

148. Thompson KM, Oldenburg WA, Deschamps C, Rupp WC,Smith CD. Chasing zero: the drive to eliminate surgical siteinfections. Ann Surg 2011;254(3):430–436.

149. Haessler S, Connelly NR, Kanter G, et al. A surgical site in-fection cluster: the process and outcome of an investigation—the impact of an alcohol-based surgical antisepsis product andhuman behavior. Anesth Analg 2010;110(4):1044–1048.

150. Panahi P, Stroh M, Casper DS, Parvizi J, Austin MS. Operatingroom traffic is a major concern during total joint arthroplasty.Clin Orthop Relat Res 2012;470(10):2690–2694.

151. Tadros MA, Williams VR, Plourde S, Callery S, Simor AE,Vearncombe M. Risk factors for Staphylococcus aureus surgical

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 22: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

strategies to prevent ssi: 2014 update 625

site infection during an outbreak in patients undergoing car-diovascular surgery. Am J Infect Control 2013;41(6):509–512.

152. Wiener-Well Y, Galuty M, Rudensky B, Schlesinger Y, AttiasD, Yinnon AM. Nursing and physician attire as possible sourceof nosocomial infections. Am J Infect Control 2011;39(7):555–559.

153. Wright SN, Gerry JS, Busowski MT, et al. Gordonia bronchialissternal wound infection in 3 patients following open heartsurgery: intraoperative transmission from a healthcare worker.Infect Control Hosp Epidemiol 2012;33(12):1238–1241.

154. Kohlenberg A, Weitzel-Kage D, van der Linden P, et al. Out-break of carbapenem-resistant Pseudomonas aeruginosa infec-tion in a surgical intensive care unit. J Hosp Infect 2010;74(4):350–357.

155. Siegel JD, Rhinehart E, Jackson M, Chiarello L; HealthcareInfection Control Practices Advisory Committee (HICPAC).Management of Multidrug-Resistant Organisms in HealthcareSettings, 2006. Atlanta: Centers for Disease Control andPrevention, 2006. http://www.cdc.gov/hicpac/pdf/MDRO/MDROGuideline2006.pdf. Accessed January 3, 2014.

156. Dodds Ashley ES, Carroll DN, Engemann JJ, et al. Risk factorsfor postoperative mediastinitis due to methicillin-resistantStaphylococcus aureus. Clin Infect Dis 2004;38(11):1555–1560.

157. Chambers D, Worthy G, Myers L, et al. Glycopeptide vs. non-glycopeptide antibiotics for prophylaxis of surgical site infec-tions: a systematic review. Surg Infect (Larchmt) 2010;11(5):455–462.

158. Bolon MK, Morlote M, Weber SG, Koplan B, Carmeli Y, WrightSB. Glycopeptides are no more effective than beta-lactamagents for prevention of surgical site infection after cardiacsurgery: a meta-analysis. Clin Infect Dis 2004;38(10):1357–1363.

159. Bull AL, Worth LJ, Richards MJ. Impact of vancomycin surgicalantibiotic prophylaxis on the development of methicillin-sen-sitive Staphylococcus aureus surgical site infections: report fromAustralian Surveillance Data (VICNISS). Ann Surg 2012;256(6):1089–1092.

160. Brennan MF, Pisters PW, Posner M, Quesada O, Shike M. Aprospective randomized trial of total parenteral nutrition aftermajor pancreatic resection for malignancy. Ann Surg 1994;220(4):436–441.

161. Veterans Affairs Total Parenteral Nutrition Cooperative StudyGroup. Perioperative total parenteral nutrition in surgical pa-tients. N Engl J Med 1991;325(8):525–532.

162. Marimuthu K, Varadhan KK, Ljungqvist O, Lobo DN. A meta-analysis of the effect of combinations of immune modulatingnutrients on outcome in patients undergoing major open gas-trointestinal surgery. Ann Surg 2012;255(6):1060–1068.

163. Zhang Y, Gu Y, Guo T, Li Y, Cai H. Perioperative immuno-nutrition for gastrointestinal cancer: a systematic review ofrandomized controlled trials. Surg Oncol 2012;21(2):e87–e95.

164. Elek SD, Conen PE. The virulence of Staphylococcus pyogenesfor man: a study of the problems of wound infection. Br J ExpPathol 1957;38(6):573–586.

165. Nakamura T, Kashimura N, Noji T, et al. Triclosan-coatedsutures reduce the incidence of wound infections and the costsafter colorectal surgery: a randomized controlled trial. Surgery2013;153(4):576–583.

166. Chang WK, Srinivasa S, Morton R, Hill AG. Triclosan-impregnated sutures to decrease surgical site infections: sys-

tematic review and meta-analysis of randomized trials. AnnSurg 2012;255(5):854–859.

167. Deliaert AE, Van den Kerckhove E, Tuinder S, et al. The effectof triclosan-coated sutures in wound healing: a double blindrandomised prospective pilot study. J Plast Reconstr Aesthet Surg2009;62(6):771–773.

168. Webster J, Alghamdi AA. Use of plastic adhesive drapes duringsurgery for preventing surgical site infection. Cochrane Data-base Syst Rev 2007;(4):CD006353.

169. Cordtz T, Schouenborg L, Laursen K, et al. The effect of in-cisional plastic drapes and redisinfection of operation site onwound infection following caesarean section. J Hosp Infect1989;13(3):267–272.

170. Dewan PA, Van Rij AM, Robinson RG, Skeggs GB, Fergus M.The use of an iodophor-impregnated plastic incise drape inabdominal surgery—a controlled clinical trial. Aust N Z J Surg1987;57(11):859–863.

171. Segal CG, Anderson JJ. Preoperative skin preparation of cardiacpatients. AORN J 2002;76(5):821–828.

172. Swenson BR, Camp TR, Mulloy DP, Sawyer RG. Antimicrobial-impregnated surgical incise drapes in the prevention of meshinfection after ventral hernia repair. Surg Infect (Larchmt) 2008;9(1):23–32.

173. Kaul AF, Jewett JF. Agents and techniques for disinfection ofthe skin. Surg Gynecol Obstet 1981;152(5):677–685.

174. Webster J, Osborne S. Preoperative bathing or showering withskin antiseptics to prevent surgical site infection. Cochrane Da-tabase Syst Rev 2007;(2):CD004985.

175. Edmiston CE Jr, Krepel CJ, Seabrook GR, Lewis BD, BrownKR, Towne JB. Preoperative shower revisited: can high topicalantiseptic levels be achieved on the skin surface before surgicaladmission? J Am Coll Surg 2008;207(2):233–239.

176. Eiselt D. Presurgical skin preparation with a novel 2% chlor-hexidine gluconate cloth reduces rates of surgical site infectionin orthopaedic surgical patients. Orthop Nurs 2009;28(3):141–145.

177. Segers P, Speekenbrink RG, Ubbink DT, van Ogtrop ML, deMol BA. Prevention of nosocomial infection in cardiac surgeryby decontamination of the nasopharynx and oropharynx withchlorhexidine gluconate: a randomized controlled trial. JAMA2006;296(20):2460–2466.

178. de Bruin AF, Gosselink MP, van der Harst E, Rutten HJ. Localapplication of gentamicin collagen implants in the prophylaxisof surgical site infections following gastrointestinal surgery: areview of clinical experience. Tech Coloproctol 2010;14(4):301–310.

179. Guzman Valdivia Gomez G, Guerrero TS, Lluck MC, DelgadoFJ. Effectiveness of collagen-gentamicin implant for treatmentof “dirty” abdominal wounds. World J Surg 1999;23(2):123–126.

180. Rutten HJ, Nijhuis PH. Prevention of wound infection in elec-tive colorectal surgery by local application of a gentamicin-containing collagen sponge. Eur J Surg Suppl 1997;(578):31–35.

181. Bennett-Guerrero E, Pappas TN, Koltun WA, et al. Genta-micin-collagen sponge for infection prophylaxis in colorectalsurgery. N Engl J Med 2010;363(11):1038–1049.

182. Eklund AM, Valtonen M, Werkkala KA. Prophylaxis of sternalwound infections with gentamicin-collagen implant: random-

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 23: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

626 infection control and hospital epidemiology june 2014, vol. 35, no. 6

ized controlled study in cardiac surgery. J Hosp Infect 2005;59(2):108–112.

183. Friberg O, Svedjeholm R, Soderquist B, Granfeldt H, VikerforsT, Kallman J. Local gentamicin reduces sternal wound infec-tions after cardiac surgery: a randomized controlled trial. AnnThorac Surg 2005;79(1):153–161.

184. Schimmer C, Ozkur M, Sinha B, et al. Gentamicin-collagensponge reduces sternal wound complications after heart sur-gery: a controlled, prospectively randomized, double-blindstudy. J Thorac Cardiovasc Surg 2012;143(1):194–200.

185. Bennett-Guerrero E, Ferguson TB Jr, Lin M, et al. Effect of animplantable gentamicin-collagen sponge on sternal wound in-fections following cardiac surgery: a randomized trial. JAMA2010;304(7):755–762.

186. Mavros MN, Mitsikostas PK, Alexiou VG, Peppas G, FalagasME. Gentamicin collagen sponges for the prevention of sternalwound infection: a meta-analysis of randomized controlledtrials. J Thorac Cardiovasc Surg 2012;144(5):1235–1240.

187. Anthony T, Murray BW, Sum-Ping JT, et al. Evaluating anevidence-based bundle for preventing surgical site infection: arandomized trial. Arch Surg 2011;146(3):263–269.

188. Young-Xu Y, Neily J, Mills PD, et al. Association between im-plementation of a medical team training program and surgicalmorbidity. Arch Surg 2011;146(12):1368–1373.

189. Malpiedi PJ, Peterson KD, Soe MM, et al. 2011 National andState Healthcare-Associated Infection Standardized Infection Ra-tio Report. Atlanta: National Center for Emerging and ZoonoticInfectious Diseases, 2013. http://www.cdc.gov/hai/pdfs/SIR/SIR-Report_02_07_2013.pdf. Accessed May 13, 2013.

190. Mu Y, Edwards JR, Horan TC, Berrıos-Torres SI, Fridkin SK.Improving risk-adjusted measures of surgical site infection forthe national healthcare safety network. Infect Control Hosp Ep-idemiol 2011;32(10):970–986.

191. Gaynes RP, Solomon S. Improving hospital-acquired infectionrates: the CDC experience. Jt Comm J Qual Improv 1996;22(7):457–467.

192. Moehring RW, Anderson DJ. “But my patients are different!”:risk adjustment in 2012 and beyond. Infect Control Hosp Ep-idemiol 2011;32(10):987–989.

193. Berrıos-Torres SI, Mu Y, Edwards JR, Horan TC, Fridkin SK.Improved risk adjustment in public reporting: coronary arterybypass graft surgical site infections. Infect Control Hosp Epi-demiol 2012;33(5):463–469.

194. Wong ES, Rupp ME, Mermel L, et al. Public disclosure ofhealthcare-associated infections: the role of the Society forHealthcare Epidemiology of America. Infect Control Hosp Ep-idemiol 2005;26(2):210–212.

195. McKibben L, Horan T, Tokars JI, et al. Guidance on publicreporting of healthcare-associated infections: recommenda-tions of the Healthcare Infection Control Practices AdvisoryCommittee. Am J Infect Control 2005;33(4):217–226.

196. Medicare program; hospital inpatient prospective payment sys-tems for acute care hospitals and the long-term care hospitalprospective payment system and FY 2012 rates; hospitals’ FTEresident caps for graduate medical education payment. Finalrules. Fed Regist 2011;76(160):51476–51846.

197. Medicare program; hospital outpatient prospective paymentsystem and CY 2007 payment rates; CY 2007 update to theambulatory surgical center covered procedures list; Medicareadministrative contractors; and reporting hospital quality data

for FY 2008 inpatient prospective payment system annual pay-ment update program—HCAHPS survey, SCIP, and mortality.Final rule with comment period and final rule. Fed Regist 2006;71(226):67959–68401.

198. National Center for Emerging and Zoonotic Infectious Diseases(NCEZID). Operational Guidance for Reporting Surgical SiteInfection (SSI) Data to CDC’s NHSN for the Purpose of FulfillingCMS’s Hospital Inpatient Quality Reporting (IQR) Program Re-quirements. Atlanta: NCEZID, 2012. http://www.cdc.gov/nhsn/PDFs/FINAL-ACH-SSI-Guidance.pdf. Accessed March 29,2013.

199. Pronovost PJ, Berenholtz SM, Needham DM. Translating evi-dence into practice: a model for large scale knowledge trans-lation. BMJ 2008;337:a1714.

200. Wick EC, Hobson DB, Bennett JL, et al. Implementation of asurgical comprehensive unit-based safety program to reducesurgical site infections. J Am Coll Surg 2012;215(2):193–200.

201. Ritter MA, French ML, Eitzen HE, Gioe TJ. The antimicrobialeffectiveness of operative-site preparative agents: a microbio-logical and clinical study. J Bone Joint Surg Am 1980;62(5):826–828.

202. The Joint Commission. Joint Commission Center for Transform-ing Healthcare: Reducing Colorectal Surgical Site Infections. Oak-brook Terrace, IL: The Joint Commission, 2013. http://www.centerfortransforminghealthcare.org/assets/4/6/SSI_storyboard.pdf. Accessed August 19, 2013.

203. The Joint Commission. The Joint Commission’s ImplementationGuide for NPSG.07.05.01 on Surgical Site Infections: The SSIChange Project. Oakbrook Terrace, IL: The Joint Commission,2013. http://www.jointcommission.org/implementation_guide_for_npsg070501_ssi_change_project/. Accessed August 19,2013.

204. Ballard MR, Miller NH, Nyquist AC, Elise B, Baulesh DM,Erickson MA. A multidisciplinary approach improves infectionrates in pediatric spine surgery. J Pediatr Orthop 2012;32(3):266–270.

205. Cima R, Dankbar E, Lovely J, et al. Colorectal surgery surgicalsite infection reduction program: a national surgical qualityimprovement program–driven multidisciplinary single-insti-tution experience. J Am Coll Surg 2013;216(1):23–33.

206. Hranjec T, Swenson BR, Sawyer RG. Surgical site infectionprevention: how we do it. Surg Infect (Larchmt) 2010;11(3):289–294.

207. Jain M, Miller L, Belt D, King D, Berwick DM. Decline in ICUadverse events, nosocomial infections and cost through a qual-ity improvement initiative focusing on teamwork and culturechange. Qual Saf Health Care 2006;15(4):235–239.

208. Alexander JW, Solomkin JS, Edwards MJ. Updated recom-mendations for control of surgical site infections. Ann Surg2011;253(6):1082–1093.

209. Hendren S, Englesbe MJ, Brooks L, Kubus J, Yin H, CampbellDA Jr. Prophylactic antibiotic practices for colectomy in Mich-igan. Am J Surg 2011;201(3):290–293.

210. Riley MM, Suda D, Tabsh K, Flood A, Pegues DA. Reductionof surgical site infections in low transverse cesarean section ata university hospital. Am J Infect Control 2012;40(9):820–825.

211. Lipke VL, Hyott AS. Reducing surgical site infections by bun-dling multiple risk reduction strategies and active surveillance.AORN J 2010;92(3):288–296.

212. Schwann NM, Bretz KA, Eid S, et al. Point-of-care electronic

This content downloaded from 24.19.122.24 on Fri, 12 Dec 2014 02:04:49 AMAll use subject to JSTOR Terms and Conditions

Page 24: Strategies to Prevent Surgical Site Infections in Acute Care Hospitals

strategies to prevent ssi: 2014 update 627

prompts: an effective means of increasing compliance, dem-onstrating quality, and improving outcome. Anesth Analg 2011;113(4):869–876.

213. Berenguer CM, Ochsner MG Jr, Lord SA, Senkowski CK. Im-proving surgical site infections: using National Surgical QualityImprovement Program data to institute Surgical Care Im-provement Project protocols in improving surgical outcomes.J Am Coll Surg 2010;210(5):737–741.

214. Kestle JR, Riva-Cambrin J, Wellons JC 3rd, et al. A standardizedprotocol to reduce cerebrospinal fluid shunt infection: the Hy-drocephalus Clinical Research Network Quality ImprovementInitiative. J Neurosurg Pediatr 2011;8(1):22–29.

215. Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG.CDC definitions of nosocomial surgical site infections, 1992:a modification of CDC definitions of surgical wound infections.Infect Control Hosp Epidemiol 1992;13(10):606–608.

216. Kaye KS, Schmit K, Pieper C, et al. The effect of increasingage on the risk of surgical site infection. J Infect Dis 2005;191(7):1056–1062.

217. Pessaux P, Msika S, Atalla D, Hay JM, Flamant Y. Risk factorsfor postoperative infectious complications in noncolorectal ab-dominal surgery: a multivariate analysis based on a prospectivemulticenter study of 4718 patients. Arch Surg 2003;138(3):314–324.

218. Raymond DP, Pelletier SJ, Crabtree TD, Schulman AM, PruettTL, Sawyer RG. Surgical infection and the aging population.Am Surg 2001;67(9):827–832.

219. Olsen MA, Lefta M, Dietz JR, et al. Risk factors for surgicalsite infection after major breast operation. J Am Coll Surg 2008;207(3):326–335.

220. Faraday N, Rock P, Lin EE, et al. Past history of skin infectionand risk of surgical site infection after elective surgery. AnnSurg 2013;257(1):150–154.

221. Forse RA, Karam B, MacLean LD, Christou NV. Antibioticprophylaxis for surgery in morbidly obese patients. Surgery1989;106(4):750–756.

222. Hawn MT, Houston TK, Campagna EJ, et al. The attributablerisk of smoking on surgical complications. Ann Surg 2011;254(6):914–920.

223. Moller AM, Pedersen T, Villebro N, Munksgaard A. Effect ofsmoking on early complications after elective orthopaedic sur-gery. J Bone Joint Surg Br 2003;85(2):178–181.

224. Moller AM, Villebro N, Pedersen T, Tonnesen H. Effect ofpreoperative smoking intervention on postoperative compli-cations: a randomised clinical trial. Lancet 2002;359(9301):114–117.

225. Sharma A, Deeb AP, Iannuzzi JC, Rickles AS, Monson JR,Fleming FJ. Tobacco smoking and postoperative outcomes aftercolorectal surgery. Ann Surg 2013;258(2):296–300.

226. Theadom A, Cropley M. Effects of preoperative smoking ces-sation on the incidence and risk of intraoperative and post-operative complications in adult smokers: a systematic review.Tob Control 2006;15(5):352–358.

227. Hennessey DB, Burke JP, Ni-Dhonochu T, Shields C, WinterDC, Mealy K. Preoperative hypoalbuminemia is an indepen-dent risk factor for the development of surgical site infectionfollowing gastrointestinal surgery: a multi-institutional study.Ann Surg 2010;252(2):325–329.

228. Boyce JM, Pittet D; Society for Healthcare Epidemiology ofAmerica, Association for Professionals in Infection Control,Infectious Diseases Society of America. Guideline for hand hy-giene in health-care settings: recommendations of the Health-care Infection Control Practices Advisory Committee and theHICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.MMWR Recomm Rep 2002;51(RR-16):1–45.

229. Ford CD, VanMoorleghem G, Menlove RL. Blood transfusionsand postoperative wound infection. Surgery 1993;113(6):603–607.

230. Horvath KA, Acker MA, Chang H, et al. Blood transfusionand infection after cardiac surgery. Ann Thorac Surg 2013;95(6):2194–2201.

231. Olsen MA, Lock-Buckley P, Hopkins D, Polish LB, Sundt TM,Fraser VJ. The risk factors for deep and superficial chest sur-gical-site infections after coronary artery bypass graft surgeryare different. J Thorac Cardiovasc Surg 2002;124(1):136–145.

232. Facility Guidelines Institute (FGI) Guidelines. ANSI/ASHRAE/ASHE Standard 170: Ventilation of Health Care Facilities. Dallas:FGI, 2010. http://www.fgiguidelines.org/guidelines2010.php.Accessed February 2, 2013.

233. Rutala WA, Weber DJ; Healthcare Infection Control PracticesAdvisory Committee (HICPAC). Guideline for Disinfection andSterilization in Healthcare Facilities, 2008. Atlanta: Centers forDisease Control and Prevention, 2008. http://www.cdc.gov/hicpac/pdf/guidelines/disinfection_nov_2008.pdf. AccessedDecember 1, 2013.

234. Guyatt GH, Oxman AD, Vist GE, et al. GRADE: an emergingconsensus on rating quality of evidence and strength of rec-ommendations. BMJ 2008;336(7650):924–926.

235. GRADE. Canadian Task Force on Preventive Health Care web-site. http://canadiantaskforce.ca/methods/grade/. Accessed De-cember 31, 2013.

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